scholarly journals Thalamic microcircuits: presynaptic dendrites form two feedforward inhibitory pathways in thalamus

2013 ◽  
Vol 110 (2) ◽  
pp. 470-480 ◽  
Author(s):  
Shane R. Crandall ◽  
Charles L. Cox
Keyword(s):  
Glutamate Receptors ◽  
Metabotropic Glutamate Receptors ◽  
Sensory Information ◽  
Activity Level ◽  
Metabotropic Glutamate ◽  
Visual Thalamus ◽  
First Response ◽  
Presynaptic Dendrites ◽  
Small Clusters ◽  
Whole Cell Recordings

In the visual thalamus, retinal afferents activate both local interneurons and excitatory thalamocortical relay neurons, leading to robust feedforward inhibition that regulates the transmission of sensory information from retina to neocortex. Peculiarly, this feedforward inhibitory pathway is dominated by presynaptic dendrites. Previous work has shown that the output of dendritic terminals of interneurons, also known as F2 terminals, are regulated by both ionotropic and metabotropic glutamate receptors. However, it is unclear whether both classes of glutamate receptors regulate output from the same or distinct dendritic terminals. Here, we used focal glutamate uncaging and whole cell recordings to reveal two types of F2 responses in rat visual thalamus. The first response, which we are calling a Type-A response, was mediated exclusively by ionotropic glutamate receptors (i.e., AMPA and NMDA). In contrast, the second response, which we are calling a Type-B response, was mediated by a combination of ionotropic and type 5 metabotropic glutamate receptors (i.e., mGluR5). In addition, we demonstrate that both F2 responses are evoked in the same postsynaptic neurons, which are morphologically distinct from neurons in which no F2 responses are observed. Since photostimulation was relatively focal and small in magnitude, these results suggest distinct F2 terminals, or small clusters of terminals, could be responsible for generating the two inhibitory responses observed. Because of the nature of ionotropic and metabotropic glutamate receptors, we predict the efficacy by which the retina communicates with the thalamus would be strongly regulated by 1) the activity level of a given retinogeniculate axon, and 2) the specific type of F2 terminals activated.

The multifaceted role of inhibitory interneurons in the dorsal lateral geniculate nucleus

2017 ◽  
Vol 34 ◽  
Author(s):  
CHARLES L. COX ◽  
JOSEPH A. BEATTY
Keyword(s):  
Glutamate Receptors ◽  
Lateral Geniculate Nucleus ◽  
Visual Information ◽  
Metabotropic Glutamate Receptors ◽  
Dorsal Lateral Geniculate Nucleus ◽  
Metabotropic Glutamate ◽  
Lateral Geniculate ◽  
Presynaptic Dendrites ◽  
Dorsal Lateral Geniculate ◽  
Stimulation Of

AbstractIntrinsic interneurons within the dorsal lateral geniculate nucleus (dLGN) provide a feed-forward inhibitory pathway for afferent visual information originating from the retina. These interneurons are unique because in addition to traditional axodendritic output onto thalamocortical neurons, these interneurons have presynaptic dendrites that form dendrodendritic synapses onto thalamocortical neurons as well. These presynaptic dendrites, termed F2 terminals, are tightly coupled to the retinogeniculate afferents that synapse onto thalamocortical relay neurons. Retinogeniculate stimulation of F2 terminals can occur through the activation of ionotropic and/or metabotropic glutamate receptors. The stimulation of ionotropic glutamate receptors can occur with single stimuli and produces a short-lasting inhibition of the thalamocortical neuron. By contrast, activation of metabotropic glutamate receptors requires tetanic activation and results in longer-lasting inhibition in the thalamocortical neuron. The F2 terminals are predominantly localized to the distal dendrites of interneurons, and the excitation and output of F2 terminals can occur independent of somatic activity within the interneuron thereby allowing these F2 terminals to serve as independent processors, giving rise to focal inhibition. By contrast, strong transient depolarizations at the soma can initiate a backpropagating calcium-mediated potential that invades the dendritic arbor activating F2 terminals and leading to a global form of inhibition. These distinct types of output, focal versus global, could play an important role in the temporal and spatial roles of inhibition that in turn impacts thalamocortical information processing.

Metabotropic glutamate receptors potentiate responses to NMDA and AMPA from layer V cells in rat visual cortex

1996 ◽  
Vol 76 (2) ◽  
pp. 808-815 ◽  
Author(s):  
X. F. Wang ◽  
N. W. Daw
Keyword(s):  
Visual Cortex ◽  
Glutamate Receptors ◽  
Metabotropic Glutamate Receptors ◽  
Nmda Antagonist ◽  
Pipette Solution ◽  
Bath Solution ◽  
Metabotropic Glutamate ◽  
Perfusion Solution ◽  
Layer V ◽  
Whole Cell Recordings

1. With the use of whole cell recordings of layer V cells from slices of rat visual cortex, we demonstrate a potentiation of the response to N-methyl-D-aspartate (NMDA) by the metabotropic glutamate agonist (1S,3R)-1-Amino-1,3-cyclopentanedicarboxylic acid. This potentiation occurs within a few seconds and lasts a few minutes. 2. The potentiation is seen with tetrodotoxin in the perfusion solution, but is abolished by guanosine 5'-O-(2-thiodiphosphate) in the pipette solution, showing that it is a postsynaptic phenomenon. The potentiation is also abolished by alpha-methyl-4-carboxyphenylglycine in the bath solution, confirming that it is due to metabotropic glutamate receptors. 3. In 29 of 31 cases tested, the response to alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid was also potentiated, and the potentiation remained in the presence of the NMDA antagonist D-2-amino-5-phosphonovalerate.

scholarly journals Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex

2014 ◽  
Vol 111 (11) ◽  
pp. 2287-2297 ◽  
Author(s):  
Tingting Liu ◽  
Iraklis Petrof ◽  
S. Murray Sherman
Keyword(s):  
Glutamate Receptors ◽  
Metabotropic Glutamate Receptors ◽  
Bathing Solution ◽  
Adjacent Layer ◽  
Metabotropic Glutamate ◽  
Group I ◽  
Mouse Cortex ◽  
Layer 4 ◽  
The Central Nervous System ◽  
Whole Cell Recordings

Metabotropic glutamate receptors (mGluRs) have a ubiquitous distribution in the central nervous system and often serve to regulate the release of neurotransmitters. We have previously shown that activation of both presynaptic and postsynaptic mGluRs can affect the gain of glutamatergic inputs in both thalamus and cortex. In the present study, we sought to determine the effect of mGluR activation on GABAergic inputs in cortex. Using whole cell recordings in a mouse slice preparation of either primary visual or auditory cortex (V1 or A1), we tested the effects on mGluRs by applying various agonists to the slice. Two pathways were tested in each area: the GABAergic inputs in layers 2/3 activated from layer 4 and the GABAergic inputs in layer 4 activated from adjacent layer 4. In both of these pathways, we found that activation of mGluRs significantly reduced the amplitude of the evoked inhibitory postsynaptic currents. Because the effects were not blocked by the addition of GDPβS to the recording electrode, and because mGluR agonists did not affect responses to photostimulation of GABA in a low-Ca2+ and high-Mg2+ bathing solution, we concluded this reduction was due to activation of presynaptic mGluRs. Furthermore, using specific mGluR agonists, we found that group II mGluRs, but not group I mGluRs, were involved in these modulatory effects. Because similar results were found in both pathways in V1 and A1, a possible cortical pattern for these effects is suggested.

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