Differential regulation of prelimbic and thalamic transmission to the basolateral amygdala by acetylcholine receptors

The amygdalar anterior basolateral nucleus (BLa) plays a vital role in emotional behaviors. This region receives dense cholinergic projections from basal forebrain which are critical in regulating neuronal activity and synaptic transmission. Cholinergic signaling in BLa is thought to occur through both a slow mode of volume transmission as well as a rapid, phasic mode. However, the relative effect of each mode of signaling in BLa is not understood. Here, we used electrophysiology and optogenetics in mouse brain slices to compare regulation of afferent input from cortex and thalamus to the BLa by these two modes of transmission. Phasic ACh release evoked by single pulse stimulation of cholinergic terminals had a biphasic effect on glutamatergic transmission at cortical input, producing rapid nicotinic receptor-mediated facilitation followed by slower muscarinic receptor (mAChR)-mediated depression. In contrast, tonic elevation of ACh through application of the cholinesterase inhibitor physostigmine suppressed glutamatergic transmission at cortical inputs through mAChRs only. This suppression was not observed at thalamic inputs to BLa. In agreement with this pathway-specificity, the mAChR agonist, muscarine more potently suppressed transmission at inputs from prelimbic cortex (PL) than thalamus. Muscarinic inhibition at PL input was dependent on presynaptic M4 mAChRs, while at thalamic input it depended upon M3 mAChR-mediated stimulation of retrograde endocannabinoid signaling. Muscarinic inhibition at both pathways was frequency-dependent, allowing only high frequency activity to pass. These findings demonstrate complex cholinergic regulation of afferent input to BLa that depends upon the mode of ACh release and is both pathway specific and frequency dependent.

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Kindling-induced long-lasting changes in synaptic transmission in the basolateral amygdala

Journal of Neurophysiology ◽

10.1152/jn.1992.67.2.443 ◽

1992 ◽

Vol 67 (2) ◽

pp. 443-454 ◽

Cited By ~ 76

Author(s):

D. G. Rainnie ◽

E. K. Asprodini ◽

P. Shinnick-Gallagher

Keyword(s):

Nmda Receptor ◽

Synaptic Transmission ◽

Basolateral Amygdala ◽

Epileptiform Activity ◽

Nmda Antagonist ◽

Burst Firing ◽

Glutamatergic Transmission ◽

Inhibitory Postsynaptic Potential ◽

Postsynaptic Potential ◽

Stimulation Of

1. Intracellular current-clamp recordings were obtained from neurons of the basolateral amygdala (BLA) in an in vitro slice preparation from control and kindled animals. Postsynaptic potentials, elicited by stimulation of the stria terminalis (ST) or lateral amygdaloid nucleus (LA), were used to investigate the role of excitatory and inhibitory amino acid transmission in kindling-induced epileptiform activity. The contributions of glutamatergic and GABAergic receptor subtypes were analyzed by use of the non-N-methyl-D-aspartate (non-NMDA) antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), the NMDA antagonist DL-2-amino-5-phosphonovaleric acid (APV), and the GABAA antagonist bicuculline methiodide (BMI). 2. The synaptic waveform evoked in control neurons consisted of an excitatory postsynaptic potential (EPSP), a fast inhibitory postsynaptic potential (f-IPSP), and a slow inhibitory postsynaptic potential (s-IPSP). Stimulation of the ST or LA pathways evoked a burst-firing response in BLA neurons contralateral from the site of stimulation of kindled animals. 3. APV (50 microM) reduced, but CNQX (10 microM) completely blocked, the burst-firing response in BLA neurons from kindled animals and bicuculline-induced bursting in control neurons. 4. Kindling significantly increased the amplitude of both the slow NMDA- and the fast non-NMDA-receptor-mediated components of synaptic transmission (s- and f-EPSPs, respectively). Furthermore, the stimulus intensities required to evoke EPSPs just subthreshold for action potential generation were significantly lower in slices from kindled animals. 5. In kindled neurons no significant change was observed in the membrane input resistance and resting membrane potential or in the number of action potentials elicited in response to depolarizating current injection. 6. Kindling resulted in a pathway-specific loss of ST- and LA-evoked feedforward GABAergic synaptic transmission and of spontaneous IPSPs. In the same BLA neurons, direct GABAergic inhibition via stimulation of the LA was not affected by kindling. 7. The enhanced glutamatergic transmission was not due to disinhibition, because, in the presence of BMI (and CNQX to prevent BMI-induced bursting), the s-EPSP amplitude was still greater in kindled than in control neurons. 8. These results provide evidence that the epileptiform activity observed in BLA neurons after kindling results from an increase in excitatory NMDA- and non-NMDA-receptor-mediated glutamatergic transmission and a decrease in inhibitory gamma-aminobutyric acid (GABA)-receptor-mediated transmission; the enhanced excitatory transmission cannot be accounted for by reduced inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)

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Facilitation of Cortico–Amygdala Synapses by Nicotine: Activity-Dependent Modulation of Glutamatergic Transmission

Journal of Neurophysiology ◽

10.1152/jn.00933.2007 ◽

2008 ◽

Vol 99 (4) ◽

pp. 1988-1999 ◽

Cited By ~ 37

Author(s):

Li Jiang ◽

Lorna W. Role

Keyword(s):

Synaptic Transmission ◽

Prenatal Exposure ◽

Long Term Potentiation ◽

Cholinergic Innervation ◽

Dependent Manner ◽

Glutamatergic Transmission ◽

Basolateral Nucleus ◽

Cortical Inputs ◽

Activity Dependent ◽

Stimulation Of

The basolateral nucleus of the amygdala (BLA) receives cholinergic innervation from the basal forebrain and nicotine, via activation of neuronal nicotinic acetylcholine receptors (nAChRs), can improve performance in amygdala-based learning tasks. We tested the hypothesis that acute and prenatal nicotine exposure modulates cortico–amygdala synaptic transmission. We found that low-dose, single-trial exposures to nicotine can elicit lasting facilitation, the extent of which is dependent on the level of stimulation of the cortical inputs to the BLA. In addition, sustained facilitation is ablated by prenatal exposure to nicotine. This study examined synaptic transmission in 238 patch-clamp recordings from BLA neurons in acute slice from mouse brain. Pharmacological studies in wild-type and nAChR subunit knock-out mice reveal that activation of presynaptic α7, containing (α7*) and non-α7* nAChRs, facilitates glutamatergic transmission in an activity-dependent manner. Without prior stimulation, application of nicotine elicits modest and transient facilitation of glutamatergic postsynaptic currents (PSCs) in about 40% of BLA neurons. With low-frequency stimulation of cortical inputs nicotine elicits robust facilitation of transmission at about 60% of cortico–BLA synapses and synaptic strength remains elevated at about 40% of these connections for >15 min after nicotine washout. Following paired-pulse stimulation nicotine elicits long-lasting facilitation of glutamatergic transmission at about 70% of cortico–BLA connections. Nicotine reduces the threshold for activation of long-term potentiation of cortico–BLA synapses evoked by patterned stimulation. Prenatal exposure to nicotine reduced subsequent modulatory responses to acute nicotine application.

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Ventral hippocampal afferents to the nucleus accumbens regulate susceptibility to depression

Nature Communications ◽

10.1038/ncomms8062 ◽

2015 ◽

Vol 6 (1) ◽

Cited By ~ 163

Author(s):

Rosemary C. Bagot ◽

Eric M. Parise ◽

Catherine J. Peña ◽

Hong-Xing Zhang ◽

Ian Maze ◽

...

Keyword(s):

Nucleus Accumbens ◽

Basolateral Amygdala ◽

Social Defeat ◽

Glutamatergic Transmission ◽

Specific Mechanism ◽

Optogenetic Stimulation ◽

Chronic Social Defeat Stress ◽

Reduced Activity ◽

Stimulation Of

Abstract Enhanced glutamatergic transmission in the nucleus accumbens (NAc), a region critical for reward and motivation, has been implicated in the pathophysiology of depression; however, the afferent source of this increased glutamate tone is not known. The NAc receives glutamatergic inputs from the medial prefrontal cortex (mPFC), ventral hippocampus (vHIP) and basolateral amygdala (AMY). Here, we demonstrate that glutamatergic vHIP afferents to NAc regulate susceptibility to chronic social defeat stress (CSDS). We observe reduced activity in vHIP in mice resilient to CSDS. Furthermore, attenuation of vHIP-NAc transmission by optogenetic induction of long-term depression is pro-resilient, whereas acute enhancement of this input is pro-susceptible. This effect is specific to vHIP afferents to the NAc, as optogenetic stimulation of either mPFC or AMY afferents to the NAc is pro-resilient. These data indicate that vHIP afferents to NAc uniquely regulate susceptibility to CSDS, highlighting an important, novel circuit-specific mechanism in depression.

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A determination of excitability changes in dorsal spinocerebellar tract neurons from spike-train analysis

Journal of Neurophysiology ◽

10.1152/jn.1977.40.3.626 ◽

1977 ◽

Vol 40 (3) ◽

pp. 626-646 ◽

Cited By ~ 19

Author(s):

C. K. Knox ◽

S. Kubota ◽

R. E. Poppele

Keyword(s):

Spike Train ◽

Afferent Input ◽

Complex Interactions ◽

Group I ◽

Long Latency ◽

Cross Correlation Analysis ◽

Output Spike ◽

Type 3 ◽

Stimulation Of

1. Responses of DSCT neurons to random electrical stimulation of peripheral nerves of the hindleg at group I intensity were studied using cross-correlation analysis of the output spike train with the stimulus. Three types of response were found: type 1 was due to monosynaptic activation of DSCT cells, type 2 resulted from inhibition of those cells, and type 3 was due to a long-latency excitation that was probably polysynaptic. 2. Most of the units studied responded to stimulation of both proximal and distal flexor and extensor nerves. The extensive convergence of afferent input on DSCT cells is much greater than has been observed previously, with type 2 and type 3 responses totaling 80% of the observed responses. We attribute this to the sensitivity of the analysis in detecting small changes in postsynaptic excitability. 3. The results of the study, particularly the derivation of postsynaptic excitability changes, generally confirm those of earlier work employing intracellular recording. 4. By varying stimulus rate and stimulus intensity in the group 1 range and simulating the resulting correlations, we conclude that excitability changes in DSCT cells are the net result of complex interactions involving excitation and inhibition. A summary of these findings is presented as a model for the minimum circuitry necessary to account for the observed behavior.

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Stimulation of Cyclic AMP Formation by Pituitary Adenylate Cyclase-Activating Polypeptide Is Attenuated by Glutamate in Rat Brain Slices

The Japanese Journal of Pharmacology ◽

10.1254/jjp.67.399 ◽

1995 ◽

Vol 67 (4) ◽

pp. 399-402

Author(s):

Kaoru Kondo ◽

Hitoshi Hashimoto ◽

Kazuko Sakata ◽

Hiroshi Saga ◽

Jun-ichi Kitanaka ◽

...

Keyword(s):

Cyclic Amp ◽

Adenylate Cyclase ◽

Rat Brain ◽

Brain Slices ◽

Pituitary Adenylate Cyclase ◽

Stimulation Of

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Preconditioning of brain slices against hypoxia induced injury by a Gynostemma pentaphyllum extract – Stimulation of anti-oxidative enzyme expression

Phytomedicine ◽

10.1016/j.phymed.2012.03.012 ◽

2012 ◽

Vol 19 (8-9) ◽

pp. 812-818 ◽

Cited By ~ 8

Author(s):

L. Schild ◽

T. Cotte ◽

G. Keilhoff ◽

R. Brödemann

Keyword(s):

Brain Slices ◽

Oxidative Enzyme ◽

Enzyme Expression ◽

Gynostemma Pentaphyllum ◽

Stimulation Of

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Growth hormone release induced by electrical stimulation of the basolateral amygdala, observed in pentobarbital anesthetized rats

Brain Research ◽

10.1016/0006-8993(86)90116-2 ◽

1986 ◽

Vol 382 (1) ◽

pp. 104-108 ◽

Cited By ~ 7

Author(s):

N. Koibuchi ◽

M. Kato ◽

T. Kakegawa ◽

M. Suzuki

Keyword(s):

Growth Hormone ◽

Electrical Stimulation ◽

Basolateral Amygdala ◽

Hormone Release ◽

Growth Hormone Release ◽

Anesthetized Rats ◽

Stimulation Of

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Frequency dependent myocardial potassium fluxes during adrenergic stimulation of intact pig hearts

Cardiovascular Research ◽

10.1093/cvr/25.5.364 ◽

1991 ◽

Vol 25 (5) ◽

pp. 364-370 ◽

Cited By ~ 4

Author(s):

O. Ellingsen ◽

O. M Sejersted ◽

O. A Vengen ◽

A. Ilebekk

Keyword(s):

Adrenergic Stimulation ◽

Frequency Dependent ◽

Stimulation Of

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Synaptic Responses of Neurons Controlling the Parotid and von Ebner Salivary Glands in Rats to Stimulation of the Solitary Nucleus and Tract

Journal of Neurophysiology ◽

10.1152/jn.01115.2007 ◽

2008 ◽

Vol 99 (3) ◽

pp. 1267-1273 ◽

Cited By ~ 8

Author(s):

Takeshi Suwabe ◽

Hideyuki Fukami ◽

Robert M. Bradley

Keyword(s):

Salivary Glands ◽

Sensory Information ◽

Salivary Secretion ◽

Afferent Input ◽

Membrane Hyperpolarization ◽

Neuron Response ◽

Glutamate Receptor Antagonists ◽

Autonomic Neurons ◽

Reflex Stimulation ◽

Stimulation Of

Salivary secretion results from reflex stimulation of autonomic neurons via afferent sensory information relayed to neurons in the rostral nucleus of the solitary tract (rNST), which synapse with autonomic neurons of the salivatory nuclei. We investigated the synaptic properties of the afferent sensory connection to neurons in the inferior salivatory nucleus (ISN) controlling the parotid and von Ebner salivary glands. Mean synaptic latency recorded from parotid gland neurons was significantly shorter than von Ebner gland neurons. Superfusion of GABA and glycine resulted in a concentration-dependent membrane hyperpolarization. Use of glutamate receptor antagonists indicated that both AMPA and N-methyl-d-aspartate (NMDA) receptors are involved in the evoked excitatory postsynaptic potentials (EPSPs). Inhibitory postsynaptic potential (IPSP) amplitude increased with higher intensity ST stimulation. Addition of the glycine antagonist strychnine did not affect the amplitude of the IPSPs significantly. The GABAA receptor antagonist, bicuculline (BMI) or mixture of strychnine and BMI abolished the IPSPs in all neurons. IPSP latency was longer than EPSP latency, suggesting that more than one synapse is involved in the inhibitory pathway. Results show that ISN neurons receive both excitatory and inhibitory afferent input mediated by glutamate and GABA respectively. The ISN neuron response to glycine probably derives from descending connections. Difference in the synaptic characteristics of ISN neurons controlling the parotid and von Ebner glands may relate to the different function of these two glands.

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