Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull

Department of Psychology and Brain Research Institute University of California, Los Angeles, CA 90024 USA
Brain Research Bulletin (Impact Factor: 2.97). 06/1986; 16(5):603-37. DOI: 10.1016/0361-9230(86)90134-6
Source: PubMed

ABSTRACT The ascending cholinergic projections of the pedunculopontine and dorsolateral tegmental nuclei, referred to collectively as the pontomesencephalotegmental (PMT) cholinergic complex, were investigated by use of fluorescent tracer histology in combination with choline-O-acetyltransferase (ChAT) immunohistochemistry and acetylcholinesterase (AChE) pharmacohistochemistry. Propidium iodide, true blue, or Evans blue was infused into the anterior, reticular, mediodorsal, central medial, and posterior nuclear areas of the thalamus; the habenula; lateral geniculate; superior colliculus; pretectal/parafascicular area; subthalamic nucleus; caudate-putamen complex; globus pallidus; entopeduncular nucleus; substantia nigra; medial septal nucleus/vertical limb of the diagonal band area; magnocellular preoptic/ventral pallidal area; and lateral hypothalamus. In some animals, separate injections of propidium iodide and true blue were made into two different regions in the same rat brain, usually a dorsal and a ventral target, in order to assess collateralization patterns. Retrogradely transported fluorescent labels and ChAT and/or AChE were analyzed microscopically on the same brain section. All of the above-delimited targets were found to receive cholinergic input from the PMT cholinergic complex, but some regions were preferentially innervated by either the pedunculopontine or dorsolateral tegmental nucleus. The former subdivision of the PMT cholinergic complex projected selectively to extrapyramidal structures and the superior colliculus, whereas the dorsolateral tegmental nucleus was observed to provide cholinergic input preferentially to anterior thalamic regions and rostral portions of the basal forebrain. The PMT cholinergic neurons showed a tendency to collateralize extensively.

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    • "MS - vDBB is known to receive inputs from the pedunculopontine tegmental nucleus and laterodorsal tegmental nucleus . These cholinergic brainstem nuclei exert influence on MS - vDBB and theta generation both via direct afferents to MS - vDBB ( Woolf and Butcher , 1986 ; Hallanger and Wainer , 1988 ) and via an indirect route through the supramammillary and posterior hypothalamic nuclei ( Kirk and McNaughton , 1991 ; Oddie et al . , 1994 ) . "
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    ABSTRACT: Neurobiological oscillations are regarded as essential to normal information processing, including coordination and timing of cells and assemblies within structures as well as in long feedback loops of distributed neural systems. The hippocampal theta rhythm is a 3-12 Hz oscillatory potential observed during cognitive processes ranging from spatial navigation to associative learning. The lower range, 3-7 Hz, can occur during immobility and depends upon the integrity of cholinergic forebrain systems. Several studies have shown that the amount of pre-training theta in the rabbit strongly predicts the acquisition rate of classical eyeblink conditioning and that impairment of this system substantially slows the rate of learning. Our lab has used a brain-computer interface that delivers eyeblink conditioning trials contingent upon the explicit presence or absence of hippocampal theta. A behavioral benefit of theta-contingent training has been demonstrated in both delay and trace forms of the paradigm with a two- to four-fold increase in learning speed. This behavioral effect is accompanied by enhanced amplitude and synchrony of hippocampal local field potentials, multiple-unit excitation, and single-unit response patterns that depend on theta state. Additionally, training in the presence of hippocampal theta has led to increases in the salience of tone-induced unit firing patterns in the medial prefrontal cortex, followed by persistent multi-unit activity during the trace interval. In cerebellum, rhythmicity and precise synchrony of stimulus time-locked local field potentials with those of hippocampus occur preferentially under the theta condition. Here we review these findings, integrate them into current models of hippocampal-dependent learning and suggest how improvement in our understanding of neurobiological oscillations is critical for theories of medial temporal lobe processes underlying intact and pathological learning.
    Frontiers in Systems Neuroscience 04/2015; DOI:10.3389/fnsys.2015.00050
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    • "Morphologically similar ChAT? neurons occur in the PPNd, but these neurons are less numerous and more widely distributed than those in the PPNc. Overall, the density of ChAT? neurons in the two parts of the PPN is lower than in the laterodorsal tegmental nucleus (LTD), a ACh brainstem nucleus that is known to innervate massively the thalamus (Sofroniew et al. 1985; Woolf and Butcher 1986; Hallanger et al. 1987; Steriade et al. 1988; Paré et al. 1988). A careful examination of coronal, sagittal and horizontal sections immunostained for ChAT has revealed that the labeled axons originating from ChAT? neurons in the PPN form a diffuse bundle that ascends within the midbrain tegmentum . "
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    ABSTRACT: The internal (GPi) and external (GPe) segments of the primate globus pallidus receive a significant cholinergic (ACh) innervation from the brainstem pedunculopontine tegmental nucleus. The present immunohistochemical study describes this innervation in the squirrel monkey (Saimiri sciureus), as visualized with an antibody raised against choline acetyltransferase (ChAT). At the light microscopic level, unbiased stereological quantification of ChAT positive (+) axon varicosities reveals a significantly lower density of innervation in GPi (0.26 ± 0.03 × 10(6)) than in GPe (0.47 ± 0.07 × 10(6) varicosities/mm(3) of tissue), with the anterior half of both segments more densely innervated than the posterior half. Neuronal density of GPi (3.00 ± 0.13 × 10(3) neurons/mm(3)) and GPe (3.62 ± 0.22 × 10(3) neurons/mm(3)) yields a mean ratio of ChAT+ axon varicosities per pallidal neuron of 74 ± 10 in the GPi and 128 ± 28 in the GPe. At the electron microscopic level, the pallidal ChAT+ axon varicosities are significantly smaller than their unlabeled counterparts, but are comparable in size and shape in the two pallidal segments. Only a minority of ChAT+ varicosities displays a synaptic specialization (12 % in the GPi and 17 % in the GPe); these scarce synaptic contacts are mostly of the symmetrical type and occur exclusively on pallidal dendrites. No ChAT+ axo-axonic synaptic contacts are observed, suggesting that ACh exerts its modulatory action on pallidal afferents through diffuse transmission, whereas pallidal neurons may be influenced by both volumic and synaptic delivery of ACh.
    Brain Structure and Function 12/2014; DOI:10.1007/s00429-014-0960-0 · 4.57 Impact Factor
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    • "Sources of ACh to exert this modulation are the PPN (Charara and Parent 1994; Mena-Segovia et al. 2004; Woolf and Butcher 1986) and some cholinergic neurons within or in the vicinity of the GPe (Bengtson and Osborne 2000; Rodrigo et al. 1998). PPN afferents also reach the Str (Dautan et al. 2014; Mena-Segovia et al. 2004; Woolf and Butcher 1986), although a main cholinergic source in this nucleus comes from interneurons (Wilson et al. 1990). "
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    ABSTRACT: The external globus pallidus (GPe) is central for basal ganglia processing. It expresses muscarinic cholinergic receptors and receives cholinergic afferents from the pedunculopontine nuclei (PPN) and other regions. The role of these receptors and afferents is unknown. Muscarinic M1-type receptors are expressed by synapses from striatal projection neurons (SPNs). Because axons from SPNs project to the GPe, one hypothesis is that striatopallidal GABAergic terminals may be modulated by M1 receptors. Alternatively, some M1 receptors may be postsynaptic in some pallidal neurons. Evidence of muscarinic modulation in any of these elements would suggest that cholinergic afferents from the PPN, or other sources, could modulate the function of the GPe. Here, we show this evidence using striatopallidal slice preparations: after field stimulation in the striatum, the cholinergic muscarinic receptor agonist, muscarine, significantly reduced the amplitude of inhibitory postsynaptic currents (IPSCs) from synapses that exhibited short-term synaptic facilitation. This inhibition was associated with significant increases in paired pulse facilitation and quantal content (CV(-2)) was proportional to IPSC amplitude. These actions were blocked by atropine, pirenzepine and mamba toxin-7; suggesting that receptors involved were M1. In addition, we found that some pallidal neurons have functional post-synaptic M1-receptors. Moreover, some evoked IPSCs exhibited short-term depression and exhibited a different kind of modulation: they were indirectly modulated by muscarine via the activation of presynaptic cannabinoid-1 receptors (CB1). Thus, pallidal synapses presenting distinct forms of short-term plasticity were modulated differently.
    Journal of Neurophysiology 11/2014; 113(3):jn.00385.2014. DOI:10.1152/jn.00385.2014 · 3.04 Impact Factor
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