ABSTRACT
Central neurons are subject to a tonic barrage of randomly occurring spontaneous inhibitory events (mIP-SCs) resulting from the action potential-independent release of gamma-aminobutyric acid (GABA). Do the terminals making synapses onto somatic versus dendritic sites, which arise from specific populations of interneurons, differ in their ability to generate mIPSCs? We have combined the techniques of whole-cell patch-clamp recording and computational simulation to demonstrate that in granule cells of the dentate gyrus, most of the action potential-independent inhibition taking place as mIPSCs originates from proximal sites. Indeed, removal of the bulk (> 50%) of the dendritic tree did not change the characteristics of mIPSCs. These results are consistent with a functional segregation of GABAergic terminals synapsing at proximal versus distal portions of central neurons. Thus, proximal GABAergic terminals are responsible for tonic inhibition targeted at the soma.
Subject(s)
Neurons/physiology , Synapses/physiology , gamma-Aminobutyric Acid/metabolism , Action Potentials , Animals , Computer Simulation , Dendrites/physiology , Electrophysiology , Kinetics , Male , Models, Biological , Nerve Endings/physiology , Neurons/ultrastructure , Patch-Clamp Techniques , Rats , Rats, WistarABSTRACT
Spontaneous neuronal activity plays an important role in the development of cortical circuitry, yet its spatio-temporal dynamics are poorly understood. Cajal-Retzius (CR) neurons in developing layer 1 are necessary for correct cortical lamination and are strategically located to coordinate early circuit activity. To characterize the spontaneous activity of CR and other layer 1 neurons during cortical development, we imaged calcium transients in populations of layer 1 neurons in hemispheres and slices from postnatal rat somato-sensory neocortex. The spontaneous activity in layer 1 had complex spatio-temporal patterns. Groups of non-CR cells showed synchronous activations and formed networks of correlated neurons superimposed in the same territory. Correlated activity among non-CR cells was mediated by a depolarizing effect of GABA and was modulated by glutamate, probably released by CR cells. Our findings demonstrate that developing layer 1 can sustain complex patterns of correlated activity and reveal a circuit mechanism that can mediate this patterned activity.
Subject(s)
Cerebral Cortex/cytology , Cerebral Cortex/growth & development , Neurons/physiology , Acetylcholine/pharmacology , Adrenergic alpha-Agonists/pharmacology , Animals , Calcium/metabolism , Electric Stimulation , Excitatory Amino Acid Agonists/pharmacology , GABA Agonists/pharmacology , Glutamic Acid/pharmacology , Muscimol/pharmacology , N-Methylaspartate/pharmacology , Neurons/chemistry , Neurotransmitter Agents/metabolism , Norepinephrine/pharmacology , Organ Culture Techniques , Patch-Clamp Techniques , Rats , Rats, Sprague-Dawley , Synaptic Transmission/drug effects , Synaptic Transmission/physiology , Tetrodotoxin/pharmacology , Time Factors , alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid/pharmacology , gamma-Aminobutyric Acid/physiologyABSTRACT
The finding that the synapses relaying sensory input to the cortex may have different properties than intracortical synapses has implications not only for sensory processing, but for the role of noise in neural computation as well.
Subject(s)
Synaptic Transmission/physiology , Animals , Cerebral Cortex/physiology , Neurons/physiologyABSTRACT
Recent studies have shown that electrical activity, particularly that mediated by NMDA receptors, has a profound effect on the development of specific neuronal connections. Blocking NMDA receptors in the ferret's lateral geniculate nucleus prevents the segregation of retinal afferents into ON and OFF sublaminae. We have now examined the involvement of NMDA receptors in the separation of afferents from the two eyes that occurs in the lateral geniculate nucleus several weeks earlier in development. Blockade of NMDA receptor activity does not appear to interfere with this eye-specific segregation.