NeuropharmacologyLayer selective presynaptic modulation of excitatory inputs to hippocampal cornu Ammon 1 by μ-opioid receptor activation
Section snippets
Preparation of hippocampal slices and staining with VSD
Use of animals in this study was approved by the Virginia Commonwealth University Institutional Animal Care and Use Committee and adhered to U.S. federal guidelines of the Animal Welfare Act and Animals Welfare Regulations and the Public Health Service Policy on Humane Care of Use of Laboratory Animals. The number of animals used in this study was limited to those necessary to show statistical differences and animals were never exposed to pain or suffering. Specifically, male Sprague–Dawley
Results
Previous studies have suggested that MOR activation can influence excitatory activity in all layers of hippocampal CA1 (McQuiston and Saggau 2003, McQuiston 2007). However, the relative effectiveness of MOR activation in the discrete layers of CA1 is not fully understood. Therefore, we performed the following experiments in an effort to determine the effect of MOR activation on excitatory activity in each anatomical layer of CA1 and to determine the synaptic location of MOR activation. First,
Discussion
This study has shown that MOR activation has direct effects in all layers of hippocampal CA1. Furthermore, the effect of MOR activation was presynaptic on inhibitory interneurons because the VSD response to direct application of GABA in all layers of CA1 was not affected by MOR activation, whereas IPSPs were suppressed by DAMGO. However, not all layers were equally affected. MOR activation had a smaller effect on EPSPs in SLM compared with all other layers. Furthermore, when comparing the
Conclusion
In conclusion, MOR activation in hippocampal CA1 had a significantly larger impact on excitatory activity in SR, SO and SP relative to SLM. These data suggest that MORs will have significant influences on inputs from CA3 pyramidal cells in SR and SO and will also facilitate firing of action potentials in pyramidal cell bodies. In contrast, MOR activation had a small effect on excitatory activity in SLM. These data point to modulation of inputs from CA3 and the output of CA1 pyramidal neurons as
Acknowledgments
The author would like to thank Karen A. Bell for her comments on this manuscript. This work was supported by a grant from NIDA R01-DA017110.
References (57)
- et al.
Autoradiographic localization of opiate receptors in rat brainIII. The telencephalon
Brain Res
(1977) - et al.
Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons
Neuron
(1992) - et al.
Conditioned place preference produced by intra-hippocampal morphine
Pharmacol Biochem Behav
(1988) - et al.
Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation
Brain Res
(1999) - et al.
Voltage-sensitive dye imaging of population neuronal activity in cortical tissue
J Neurosci Methods
(2002) - et al.
Dissociation of mu and delta opioid receptor-mediated reductions in evoked and spontaneous synaptic inhibition in the rat hippocampus in vitro
Brain Res
(1992) - et al.
Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS
J Chem Neuroanat
(1995) - et al.
mu-Opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding
Brain Res
(1994) - et al.
Chronic in vivo morphine administration facilitates primed-bursts-induced long-term potentiation of Schaffer collateral-CA1 synapses in hippocampal slices in vitro
Brain Res
(1999) - et al.
Augmentation of LTP induced by primed-bursts tetanic stimulation in hippocampal CA1 area of morphine dependent rats
Brain Res
(1997)
Enkephalin inhibition of inhibitory input to CA1 and CA3 pyramidal neurons in the hippocampus
Brain Res
Differences between somatic and dendritic inhibition in the hippocampus
Neuron
Involvement of NMDA receptors and voltage-dependent calcium channels on augmentation of long-term potentiation in hippocampal CA1 area of morphine dependent rats
Brain Res
Pertussis toxin attenuates intracranial morphine self-administration
Pharmacol Biochem Behav
Hippocampal mu-receptors mediate opioid reinforcement in the CA3 region
Brain Res
Comparison of opioid and GABA receptor control of excitability and membrane conductance in hippocampal CA1 pyramidal cells in rat
Neuropharmacology
Chronic morphine exposure blocks opioid effects on both the early and late inhibitory postsynaptic potentials in hippocampal CA1 pyramidal cells
Neurosci Lett
Opioids activate both an inward rectifier and a novel voltage-gated potassium conductance in the hippocampal formation
Neuron
Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies
J Neurosci
Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord
J Neurosci
Colocalization of mu opioid receptors with GIRK1 potassium channels in the rat brain: an immunocytochemical study
Receptors Channels
Mechanism of mu-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro
J Physiol
Presynaptic inhibition of calcium-dependent and -independent release elicited with ionomycin, gadolinium, and alpha-latrotoxin in the hippocampus
J Neurophysiol
Quantitative autoradiographic analysis of mu and delta opioid binding sites in the rat hippocampal formation
J Comp Neurol
Immunohistochemical localization of mu-opioid receptors in the central nervous system of the rat
J Comp Neurol
Mu opioid receptors are in discrete hippocampal interneuron subpopulations
Hippocampus
Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing
J Neurophysiol
Disruption of synchronous gamma oscillations in the rat hippocampal slice: a common mechanism of anaesthetic drug action
Br J Pharmacol
Cited by (17)
HIV-1 Tat reduces apical dendritic spine density throughout the trisynaptic pathway in the hippocampus of male transgenic mice
2022, Neuroscience LettersCitation Excerpt :Although spine density along the trisynaptic pathway was unaltered by 2 weeks of morphine exposure, morphine may affect other aspects of hippocampal structure and function since CA3 pyramidal neurons, interneuronal subpopulations or their synaptic projections [47], and subsets of glia including astrocytes [13,23,48,62,66] express μ-opioid receptors (MORs). For example, the MOR agonist [D-Ala2, N-MePhe4, Gly-ol]-enkephalin (DAMGO) markedly increases CA1 pyramidal cell excitability via MOR-expressing subsets of interneurons in the stratum pyramidale and oriens of CA1 [42,43]. In the oriens-lacunosum moleculare, MOR activation can modulate presynaptic mossy fiber inputs to CA3 pyramidal cells [23] and microinjecting the irreversible MOR antagonist β-funaltrexamine into CA3 blocks spatial learning [44].
Mu opioid receptor activation normalizes temporo-ammonic pathway driven inhibition in hippocampal CA1
2011, NeuropharmacologyCitation Excerpt :We have previously shown that activation of TA afferents 200 ms before SC stimulation resulted in an inhibition of SC EPSPs in SR and SP of hippocampal CA1 (McQuiston, 2010). Because MOR activation partially blocks monosynaptic IPSPs in SR and SP of hippocampal CA1 (McQuiston, 2007; McQuiston, 2008; McQuiston and Saggau, 2003), we next examined the effect that the activation of MORs has on the integrative properties between TA and SC afferents in hippocampal CA1 when SC stimulation was delayed by 200 ms. When TA was stimulated 200 ms before SC, the amplitude of EPSPs in SR (purple) and SP (dark blue) were smaller relative to EPSPs evoked by SC stimulation alone (SR – red, SP – light blue, Fig. 3A).
Endogenous opiates and behavior: 2008
2009, PeptidesCitation Excerpt :Prenatal morphine exposure attenuated the maintenance of late LTP in lateral perforant path projections to the dentate gyrus and the hippocampal CA3 region [986]. Layer selective presynaptic activation of excitatory inputs to hippocampal cornu Ammon 1 were observed by MOR activation in the strata radiatum, pyramidale and oriens, but not the lacunosum-moleculare [649]. Endogenous opioids inhibited ischemia-induced generation of immature hippocampal neurons as demonstrated in MOR KO mice [510].
Neuropeptides in depression: Role of VGF
2009, Behavioural Brain ResearchCell-Type Specific Inhibition Controls the High-Frequency Oscillations in the Medial Entorhinal Cortex
2022, International Journal of Molecular Sciences