Possible Functional Roles of the Bipartite Dendrites of Pyramidal Cells

GABAA-Mediated IPSCs in Piriform Cortex Have Fast and Slow Components With Different Properties and Locations on Pyramidal Cells

Journal of Neurophysiology ◽

10.1152/jn.1997.78.5.2531 ◽

1997 ◽

Vol 78 (5) ◽

pp. 2531-2545 ◽

Cited By ~ 49

Author(s):

A. Kapur ◽

R. A. Pearce ◽

W. W. Lytton ◽

L. B. Haberly

Keyword(s):

Time Course ◽

Feedback Inhibition ◽

Slow Component ◽

Piriform Cortex ◽

Pyramidal Cells ◽

Long Term Potentiation ◽

Companion Paper ◽

Protective Role ◽

Functional Roles ◽

Term Potentiation

Kapur, A., R. A. Pearce, W. W. Lytton, and L. B. Haberly.GABAA-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J. Neurophysiol. 78: 2531–2545, 1997. A recent study in piriform (olfactory) cortex provided evidence that, as in hippocampus and neocortex, γ-aminobutyric acid-A (GABAA)-mediated inhibition is generated in dendrites of pyramidal cells, not just in the somatic region as previously believed. This study examines selected properties of GABAA inhibitory postsynaptic currents (IPSCs) in dendritic and somatic regions that could provide insight into their functional roles. Pharmacologically isolated GABAA-mediated IPSCs were studied by whole cell patch recording in slices. To compare properties of IPSCs in distal dendritic and somatic regions, local stimulation was carried out with tungsten microelectrodes, and spatially restricted blockade of GABAA-mediated inhibition was achieved by pressure-ejection of bicuculline from micropipettes. The results revealed that largely independent circuits generate GABAA inhibition in distal apical dendritic and somatic regions. With such independence, a selective decrease in dendritic-region inhibition could enhance integrative or plastic processes in dendrites while allowing feedback inhibition in the somatic region to restrain system excitability. This could allow modulatory fiber systems from the basal forebrain or brain stem, for example, to change the functional state of the cortex by altering the excitability of interneurons that mediate dendritic inhibition without increasing the propensity for regenerative bursting in this highly epileptogenic system. As in hippocampus, GABAA-mediated IPSCs were found to have fast and slow components with time constants of decay on the order of 10 and 40 ms, respectively, at 29°C. Modeling analysis supported physiological evidence that the slow time constant represents a true IPSC component rather than an artifactual slowing of the fast component from voltage clamp of a dendritic current. The results indicated that, whereas both dendritic and somatic-region IPSCs have both fast and slow GABAA components, there is a greater proportion of the slow component in dendrites. In a companion paper, the hypothesis is explored that the resulting slower time course of the dendritic IPSC increases its capacity to regulate the N-methyl-d-aspartate component of EPSPs. Finally, evidence is presented that the slow GABAA-mediated IPSC component is regulated by presynaptic GABAB inhibition whereas the fast is not. Based on the requirement for presynaptic GABAB-mediated block of inhibition for expression of long-term potentiation, this finding is consistent with participation of the slow GABAA component in regulation of synaptic plasticity. The lack of susceptibility of the fast GABAA component to the long-lasting, activity-induced suppression mediated by presynaptic GABAB receptors is consistent with a protective role for this process in preventing seizure activity.

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Synaptic Connectivity of Distinct Hilar Interneuron Subpopulations

Journal of Neurophysiology ◽

10.1152/jn.1998.79.6.3229 ◽

1998 ◽

Vol 79 (6) ◽

pp. 3229-3237 ◽

Cited By ~ 8

Author(s):

Matteo Forti ◽

Hillary B. Michelson

Keyword(s):

Morphological Characteristics ◽

Pyramidal Cells ◽

Synaptic Connectivity ◽

Postsynaptic Potentials ◽

Functional Roles ◽

Inhibitory Postsynaptic Potentials ◽

Projection Properties ◽

Inhibitory Circuit ◽

Ca3 Pyramidal Cells ◽

Dentate Hilus

Forti, Matteo and Hillary B. Michelson. Synaptic connectivity of distinct hilar interneuron subpopulations. J. Neurophysiol. 79: 3229–3237, 1998. Dual intracellular recordings of hilar interneurons and CA3 pyramidal cells were performed in transverse slices of guinea pig hippocampus in the presence of the convulsant compound 4-aminopyridine (4-AP) and ionotropic glutamate receptor antagonists. Under these conditions, interneurons burst fire synchronously, producing synchronized inhibitory postsynaptic potentials (sIPSPs) in pyramidal cells. Three different hilar interneuron subpopulations that contributed to the sIPSP were identified based on their projection properties and morphology. These three types were pyramidal-like stellate interneurons, spheroid interneurons, and oviform interneurons. Physiologically, pyramidal-like stellate interneurons could be differentiated from the other interneuron subpopulations because they generated short synchronized bursts of action potentials coincident with the hyperpolarizing and depolarizing γ-aminobutyric acid-A (GABAA)-mediated inhibitory postsynaptic potentials (IPSPs) recorded in pyramidal cells. The bursts in pyramidal-like stellate cells were abolished by theGABAA-receptor blocker, bicuculline. In contrast, spheroid interneurons of the dentate-hilus (D-H) border and oviform hilar interneurons exhibited prolonged bicuculline-resistant bursts that occurred coincident with the GABAB pyramidal cell sIPSPs. Pyramidal-like stellate interneurons likely did not contribute to the generation of synchronized GABAB responses in hippocampal pyramidal cells. Spheroid interneurons were unique among these subpopulations of interneurons in that the bicuculline-resistant bursts in spheroid interneurons were sustained by a synaptic depolarization that persisted in the presence of antagonists of ionotropic glutamate, GABAA and GABAB receptors [6-cyano-7-nitroquinoxaline-2,3-dione, 20 μM; 3-3(2-carboxipiperazine-4-yl)propyl-1-phosphonate, 20 μM; bicuculline, 10–15 μM; CGP 55845A, 20 μM]. This novel depolarizing potential reversed between −30 and 0 mV. No noticeable synaptic depolarization sustaining burst firing could be isolated in oviform interneurons, suggesting that firing in this interneuron subpopulation was synchronized by nonsynaptic mechanisms. The results of the present study indicate that the hilar inhibitory circuit is composed of at least three different subpopulations of interneurons, distinguishable by their morphological characteristics and synaptic inputs and outputs. These findings give further support to the hypothesis that there are distinct populations of interneurons producing GABAA and GABAB responses with defined functional roles within the hippocampal inhibitory circuit. Notably, we found that spheroid interneurons were unique among the hilar interneurons studied, in that the synchronized bursts observed in these cells are sustained by a novel ionotropic glutamate and GABA receptor-independent synaptic depolarization.

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Kinetics of Fast Short-Term Depression Are Matched to Spike Train Statistics to Reduce Noise

Journal of Neurophysiology ◽

10.1152/jn.00117.2010 ◽

2010 ◽

Vol 103 (6) ◽

pp. 3337-3348 ◽

Cited By ~ 8

Author(s):

Reza Khanbabaie ◽

William H. Nesse ◽

Andre Longtin ◽

Leonard Maler

Keyword(s):

Pyramidal Cells ◽

Short Term ◽

Unit Discharge ◽

Functional Roles ◽

Afferent Fibers ◽

Mean And Variance ◽

The Mean ◽

Discharge Patterns ◽

Kinetics Of ◽

Synaptic Responses

Short-term depression (STD) is observed at many synapses of the CNS and is important for diverse computations. We have discovered a form of fast STD (FSTD) in the synaptic responses of pyramidal cells evoked by stimulation of their electrosensory afferent fibers (P-units). The dynamics of the FSTD are matched to the mean and variance of natural P-unit discharge. FSTD exhibits switch-like behavior in that it is immediately activated with stimulus intervals near the mean interspike interval (ISI) of P-units (∼5 ms) and recovers immediately after stimulation with the slightly longer intervals (>7.5 ms) that also occur during P-unit natural and evoked discharge patterns. Remarkably, the magnitude of evoked excitatory postsynaptic potentials appear to depend only on the duration of the previous ISI. Our theoretical analysis suggests that FSTD can serve as a mechanism for noise reduction. Because the kinetics of depression are as fast as the natural spike statistics, this role is distinct from previously ascribed functional roles of STD in gain modulation, synchrony detection or as a temporal filter.

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