Serotonin-immunoreactive projections to the hippocampus from the interpeduncular nucleus in the rat

doi:10.1016/0304-3940(86)90338-1

Neuroscience Letters

Volume 64, Issue 3, 14 March 1986, Pages 259-262

https://doi.org/10.1016/0304-3940(86)90338-1 Get rights and content

Abstract

The possibility of a serotonergic projection from the interpeduncular nucleus (IPN) to the hippocampus was examined using a combined immunohistochemical-fluorescence retrograde tracing technique. About one third of the cells in the apical subnucleus of the IPN which projected to the hippocampus could be shown to contain serotonin immunoreactivity, whereas double-labeled cells were only rarely encountered in the lateral subnuclei. These findings suggest that the IPN sends both serotonergic and non-serotonergic projections to the hippocampus and that the serotonergic projections arise primarily from the apical subnucleus.

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Cited by (18)

Temporary inactivation of interpeduncular nucleus impairs long but not short term plasticity in the perforant-path dentate gyrus synapses in rats
2020, Behavioural Brain Research
Citation Excerpt :
However, the ways that these projections terminate to either the DG granular cells or GABAergic interneurons through the excitatory/inhibitory projections still remains to be investigated. On the other hand, IPN could act on the hippocampus through several structures which are involved in the hippocampal dependent learning and memory processes and theta rhythm activity including raphe nuclei, nucleus incertus, septum and supra mammillary nucleus [21,23,24,38,39]. In Fig. 10, we proposed a diagrammatic reconstruction of these direct and indirect pathways from IPN to the hippocampus.
The interconnectivity of the hippocampus, interpeduncular nucleus (IPN) and several brain structures which are involved in modulating hippocampal theta rhythm activity makes a complicated dynamic network of interconnected regions and highlights the role of IPN in the hippocampal dependent learning and memory. In the present study we aimed to address whether IPN is involved in the perforant path-dentate gyrus (PPDG) short term and long term synaptic plasticity in rats. To silent IPN transiently, lidocaine was injected through the implanted cannula above the IPN. To evaluate short term plasticity, paired pulses stimulation of PPDG synapses were used upon IPN temporary inactivation. Furthermore, long term plasticity was investigated by measuring the induction and maintenance of PPDG synapses long term potentiation (LTP) after high frequency stimulation (HFS) of the mentioned pathway following to IPN inactivation. The results showed that IPN reversible inactivation had no effect on short term plasticity of PPDG synapses. However, IPN inactivation before the PPDG high frequency stimulation could significantly suppress both the population spike (PS) and fEPSP-LTP induction compared to the saline group. Conversely, IPN inactivation had no significant effect on maintenance of both PS-LTP and fEPSP-LTP. All together our study suggests the contribution of IPN in the PPDG synaptic plasticity and excitability of DG granule cells which could be through direct and/or indirect pathways from IPN to the hippocampus.
Reversible inactivation of interpeduncular nucleus impairs memory consolidation and retrieval but not learning in rats: A behavioral and molecular study
2018, Behavioural Brain Research
Citation Excerpt :
Previous studies in our laboratory investigated how different structurally-connected areas with hippocampus could change the quality of learning and memory formation via their own specific underlying mechanisms [8,19,39–41]. The existence of direct and indirect anatomical connections between the IPN and hippocampus suggests that these two structures are functionally related [4,13,30,42,51]. Thus, in the present study, we aimed to determine whether IPN acts as a modulator of hippocampal dependent learning and memory processes.
The Interpedundular nucleus (IPN) is a small midbrain structure located deeply between the two cerebral peduncles. The strategic placement of this nucleus makes it a possible relay between structures involved in the modulation of hippocampal theta rhythm activity. In this study we aimed to investigate how reversible inactivation of IPN could affect the acquisition, consolidation and retrieval phases of memory in passive avoidance (PA) and Morris water maze (MWM) tasks. To support our data, molecular studies were performed in order to detect possible changes in the expression of proteins related to learning and memory in the hippocampus. To address this issue rats’ IPN was reversibly inactivated by microinjection of lidocaine hydrochloride (4%). After the behavioral studies, the phosphorylation of CREB and P70, and c-fos expression levels in the hippocampus were determined using western blotting and immunohistochemistry respectively. Our results in the PA and MWM tasks showed that IPN reversible inactivation could impair immediate post training consolidation and retrieval while it had no effect on the acquisition phase. In addition, there was a deficit in the retention of the MWM working memory. Our data showed the ratio of pCREB/CREB, pP70/P70 and c-fos expression in the hippocampus significantly decreased after IPN reversible inactivation. Collectively, the results show that behaviorally defined changes could be due to what happens molecularly in the hippocampus after IPN reversible inactivation. It is concluded that IPN not only makes part of a network involved in the modulation of hippocampal theta rhythm activity, but also is actively engaged in hippocampal memory formation.
The fasciculus retroflexus controls the integrity of REM sleep by supporting the generation of hippocampal theta rhythm and rapid eye movements in rats
1998, Brain Research Bulletin
The fasciculus retroflexus (FR) fiber bundle comprises the intense cholinergic projection from the medial division of the habenula nucleus (Hbn) of the epithalamus to the interpeduncular nucleus (IPN) of the limbic midbrain. Due to the widespread connections of the Hbn and IPN, it could be surmised that the FR is integrated in the processings of various subsystems that are known to be involved in the sleep–wake mechanisms; relevant sites include the limbic forebrain and midbrain areas and more caudal pontine structures. Consequently, the present study addressed the significance of the FR in the spontaneous sleep–wake stage-associated variations of the different activity patterns of frontal cortex and hippocampal electroencephalograms (EEGs), the electrooculogram, and body movements, in freely behaving rats that had been subjected to either bilateral electrolytic lesioning of the FR or control operations. The evolution of different state combinations was assessed by the combinatory analysis of different activity stages appearing on the 6-h records. As compared to the control-operated group, the FR lesioning substantially reduced the time spent in rapid eye movement (REM) sleep by 79%, moderately decreased the duration of the intermediate state of sleep by 29%, and quiet waking state by 44%, but had virtually no effects on the durations of different types of non-REM sleep (i.e., drowsiness that which involved quiet sleep or slow-wave sleep containing delta and spindle state components) or on the times of active waking behavior that corresponded to the body movements. Quantitative decomposition analyses revealed marked variations in the frontal cortex and hippocampal activity as well as REM during the course of the extracted sleep–wake stages described and there were also some group differences. Of those individual features that were used to determine different sleep–wake stages, the overall hippocampal theta time (41% decrease) and single REM frequency (71% reduction during the REM sleep) were most affected. In contrast, the various properties of desynchronization/synchronization patterns of frontal cortex EEGs were consistently hardly influenced by the FR lesioning. Therefore, the present data suggest the involvement of the FR in the REM sleep processes by establishing prominent associations with the limbic and REM control mechanisms that involve the hippocampus and plausibly pontine ocular activity networks.
Habenulo-interpeduncular descending pathways and their relationship to enkephalin- and somatostatin-immunoreactive neurons in the interpeduncular nucleus of human fetuses
1993, Neuroscience
The interpeduncular nucleus of six human fetuses aged 15 (one specimen), 26 (one specimen), 38 (one specimen) and 40 (three specimens) gestation weeks was studied by immunohistochemistry for enkephalin and somatostatin localization and immunohistochemistry coupled with silver staining. Enkephalin-positive and somatostatin-positive cells were detected, the former initially at 15 weeks gestation and the latter at 26 weeks gestation. They appeared to receive long afferents from the habenular region and projected short efferents to adjacent cells devoid of enkephalin and somatostatin positivity.
We postulate that these enkephalin- and somatostatin-positive neurons function as modulatory interneurons in the habenulo-interpeduncular and related pathways.
Ultrastructural features of the serotonin innervation in adult rat hippocampus: An immunocytochemical description in single and serial thin sections
1991, Neuroscience
This study was aimed at characterizing the fine-structural features of the normal serotonin (5-HT) innervation in adult rat hippocampus, by means of electron microscopic immunocytochemistry with a polyclonal antiserum against 5-HT-glutaraldehyde-protein conjugate (donated by Michel Geffard, Bordeaux). Two hippocampal sectors were examined, at mid-level along the septo-temporal axis: CA3-a of Ammon's horn and crest of the dentate gyrus (DG-c). A large number of axonal varicosities (terminals) were sampled in single ultrathin sections, to achieve a statistically significant comparison of their size and of their relative frequency of synaptic specialization, junctional targets and juxtaposed elements, between the oriens and the radiatum layer of CA3-a, and the molecular and the polymorph layer of DG-c. In both CA3-a layers, the microenvironment of the immunostained terminals was also compared to that of a population of unlabeled varicosities randomly selected from the same micrographs. Moreover, 57 varicosities from the oriens and the radiatum layer of CA3-a were visualized in a long series of thin sections, allowing for their examination from end to end in 43 instances. As measured in single sections, hippocampal 5-HT varicosities were of comparable diameter (0.57 μm on the average) in the two anatomical sectors and four neuropil layers examined. As extrapolated stereologically to whole varicosities, the proportion making a synaptic membrane specialization (synaptic incidence) ranged from 18 to 33% (average of 24%), without statistically significant differences between the two sectors and four layers. The synaptic incidence determined directly from serial sections of CA3-a (18%) was nearly identical to that extrapolated from single sections (18.1% in the oriens and 19.5% in the radiatum layer). In both CA3-a and DG-c, the 5-HT varicosities showing a junctional complex were slightly larger than their non-junctional counterparts. In CA3-a, only dendritic shafts were targeted by synaptic 5-HT varicosities, whereas in DG-c there were also a few axo-spinous synapses. The microenvironment of CA3-a 5-HT varicosities differed markedly from that of randomly selected unlabeled varicosities, due to its much lower frequency of synaptic targets and higher frequency of juxtaposed axonal varicosities, at least in the radiatum layer. In all four layers examined, other axonal varicosities were indeed the most frequently encountered neuronal element in the immediate vicinity of immunostained 5-HT varicosities. Neurites and dendritic shafts were also common, but dendritic spines (4%) were relatively infrequent.
Thus, the normal 5-HT innervation of adult rat hippocampus is predominantly non-junctional (70–80% of its varicosities), and it exhibits comparable intrinsic and relational features in the four neuropil layers of CA3-a and DG-c.
Substance P immunoreactivity in the rat interpeduncular nucleus: Synaptic interactions between substance P-positive profiles and choline acetyltransferase- or glutamate decarboxylase-immunoreactive structures
1991, Neuroscience
The subnuclear and synaptic distribution of substance P immunoreactivity was examined in the rat interpeduncular nucleus at the light and electron microscope level. The nucleus possessed a prominent substance P-immunoreactive axonal plexus in the lateral and dorsomedial subnuclei and in the dorsal cap of the rostral subnucleus. The density of substance P-immunoreactive axons in the remaining subnuclear divisions was sparse to moderate. Terminals of immunoreactive axons contained spherical vesicles and formed asymmetric contacts on dendritic processes exclusively. Immunoreactive neurons, restricted to the rostral subnucleus, possessed long, sparsely branched dendrites. Unlabelled terminals containing either spherical or pleomorphic vesicles contacted substance P-immunoreactive dendritic profiles. Axodendritic and axosomatic synapses containing substance P immunoreactivity pre- and postsynaptically were not observed. Ultrastructural evidence for synaptic relationships between substance P-containing profiles and those containing either choline acetyltransferase or glutamate decar☐ylase was obtained by means of double antigen immunohistochemistry. Terminals of fasciculus retroflexus axons stained for choline acetyltransferase immunoreactivity formed asymmetric synaptic contacts with substance P-immunoreactive dendritic profiles. Few substance P-positive dendrites in the rostral subnucleus received terminals possessing glutamate decar☐ylase activity. Unlabelled terminals containing either spherical or pleomorphic vesicles contacted substance P- and glutamate decar☐ylase-immunoreactive dendritic profiles simultaneously. Terminals possessing either substance P or glutamate decar☐ylase immunoreactivity formed synaptic contacts with dendritic processes of neurons in the lateral subnucleus. Many of the neurons within this subnuclear division contained glutamate decar☐ylase.
This study provides direct evidence of synaptic relationships between choline acetyltransferase-immunoreactive axons and substance P-immunoreactive dendritic profiles and between substance P-positive axons and glutamate decar☐ylase-immunoreactive dendrites. These findings reveal that two types of transmitter-specific axons of the fasciculus retroflexus innervate neuronal populations of the interpeduncular nucleus stained immunohistochemically for either substance P or glutamate decar☐ylase.

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Serotonin-immunoreactive projections to the hippocampus from the interpeduncular nucleus in the rat

Abstract

Neurosci. Lett.

Brain Res. Bull.

Neuroscience

Brain Res. Bull.

Brain Res. Bull.

Brain Res.