An Analysis of the Adaptive Behavior of Piriform Cortex Pyramidal Cells

1. Intracellular recordings were obtained from anatomically verified layer II pyramidal cells in slices from rat piriform cortex cut perpendicular to the surface. 2. Responses to afferent and association fiber stimulation at resting membrane potential consisted of a depolarizing potential followed by a late hyperpolarizing potential (LHP). Membrane polarization by current injection revealed two components in the depolarizing potential: an initial excitatory postsynaptic potential (EPSP) followed at brief latency by an inhibitory postsynaptic potential (IPSP) that inverted with membrane depolarization and truncated the duration of the EPSP. 3. The early IPSP displayed the following characteristics suggesting mediation by gamma-aminobutyric acid (GABA) receptors linked to Cl- channels: associated conductance increase, sensitivity to increases in internal Cl- concentration, blockage by picrotoxin and bicuculline, and potentiation by pentobarbital sodium. The reversal potential was in the depolarizing direction with respect to resting membrane potential so that the inhibitory effect was exclusively via current shunting. 4. The LHP had an associated conductance increase and a reversal potential of -90 mV in normal bathing medium that shifted according to Nernst predictions for a K+ potential with changes in external K+ over the range 4.5-8 mM indicating mediation by the opening of K+ channels and ruling out an electrogenic pump origin. 5. Lack of effect of bath-applied 8-bromoadenosine 3',5'-cyclic monophosphate (8-Br-cAMP) or internally applied ethylene glycol-bis(beta-aminoethyl ether)-N,N,N',N'-tetraacetic acid (EGTA) on the LHP and failure of high amplitude, direct membrane depolarization to evoke a comparable potential, argue against endogenous mediation of the LHP by a Ca2+ activated K+ conductance [gK(Ca)]. However, an apparent endogenously mediated gK(Ca) with a duration much greater than the LHP was observed in a low percent of layer II pyramidal cells. Lack of effect of 8-Br-cAMP also indicates a lack of dependence of the LHP on cAMP. 6. Other characteristics of the LHP that were demonstrated include: a lack of blockage by GABAA receptor antagonists, a probable voltage sensitivity (decrease in amplitude in the depolarizing direction), and an apparent brief onset latency (less than 10 ms) when the early IPSP was blocked by picrotoxin. The LHP was unaffected by pentobarbital sodium when the early IPSP was blocked by picrotoxin. 7. Both the LHP and early IPSP were blocked by low Ca2+/high Mg2+, consistent with disynaptic mediation.(ABSTRACT TRUNCATED AT 400 WORDS)

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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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Spike Coding in Pyramidal Cells of the Piriform Cortex of Rat

Journal of Neurophysiology ◽

10.1152/jn.2001.86.3.1504 ◽

2001 ◽

Vol 86 (3) ◽

pp. 1504-1510 ◽

Cited By ~ 8

Author(s):

Alexander D. Protopapas ◽

James M. Bower

Keyword(s):

Cognitive Function ◽

Piriform Cortex ◽

Pyramidal Cells ◽

Spike Trains ◽

Gamma Range ◽

Cortical Oscillations ◽

Cell Recording ◽

Spike Coding ◽

Theta Range

The study of cortical oscillations has undergone a renaissance in recent years because of their presumed role in cognitive function. Of particular interest are frequencies in the gamma (30–100 Hz) and theta (3–12 Hz) ranges. In this paper, we use spike coding techniques and in vitro whole cell recording to assess the ability of individual pyramidal cells of the piriform cortex to code inputs occurring in these frequencies. The results suggest that the spike trains of individual neurons are much better at representing frequencies in the theta range than those in the gamma range.

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Transient synaptic modifications in piriform cortex pyramidal cells associated with odor learning

Neuroscience Letters ◽

10.1016/s0304-3940(97)90176-2 ◽

1997 ◽

Vol 237 ◽

pp. S43

Author(s):

D. Saar ◽

D. Lebel ◽

Y. Grossman ◽

E. Barkai

Keyword(s):

Piriform Cortex ◽

Pyramidal Cells ◽

Odor Learning

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New Features of Connectivity in Piriform Cortex Visualized by Intracellular Injection of Pyramidal Cells Suggest that “Primary” Olfactory Cortex Functions Like “Association” Cortex in Other Sensory Systems

Journal of Neuroscience ◽

10.1523/jneurosci.20-18-06974.2000 ◽

2000 ◽

Vol 20 (18) ◽

pp. 6974-6982 ◽

Cited By ~ 208

Author(s):

Dawn M. G. Johnson ◽

Kurt R. Illig ◽

Mary Behan ◽

Lewis B. Haberly

Keyword(s):

Piriform Cortex ◽

Pyramidal Cells ◽

Sensory Systems ◽

Olfactory Cortex ◽

Association Cortex ◽

Intracellular Injection ◽

Primary Olfactory Cortex

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Afferent and association fiber differences in short-term potentiation in piriform (olfactory) cortex of the rat

Journal of Neurophysiology ◽

10.1152/jn.1990.64.1.179 ◽

1990 ◽

Vol 64 (1) ◽

pp. 179-190 ◽

Cited By ~ 17

Author(s):

M. E. Hasselmo ◽

J. M. Bower

Keyword(s):

Time Constant ◽

Piriform Cortex ◽

Low Frequency ◽

Pyramidal Cells ◽

Olfactory Cortex ◽

Short Term ◽

Term Potentiation ◽

Association Fibers ◽

Stimulation Of

1. The effects of low-frequency stimulus trains on synaptically evoked responses in piriform cortex pyramidal cells were studied by the use of intracellular recording techniques in an in vitro slice preparation. Afferent and association fiber systems were differentially stimulated with electrodes placed in layer 1a or layer 1b, respectively. To quantify synapse modifiability, the heights of postsynaptic potentials (PSPs) elicited by paired-pulse stimulation (100-ms interval) were averaged over a 50-s period before and after a set of 10 stimulus trains (10 pulses each, 20 Hz, 5-s interpulse interval). 2. Afferent and association fibers showed consistent differences in their response to stimulation during the period lasting from approximately 10 to 200 s after presentation of trains. During this time period, the responses to stimulation of association fibers in layer 1b displayed a short-term potentiation, which over the 10 posttrain trials, produced an average increase in PSP height of 23.2 +/- 3.7% (mean +/- SE). On the other hand, responses to layer 1a stimulation showed an average depression of 10.9 +/- 3.6%. Layer 1b potentiation decayed with time constant roughly estimated at 79 s. Layer 1b potentiation appeared even at very low stimulus voltages and after local association fiber input had been cut, suggesting that it was largely a monosynaptic effect. 3. In the period immediately after train presentations, responses evoked by both layers showed a short-term augmentation with a time constant around 3 s. In layer 1a, this augmentation was superimposed on a depression with slow recovery. At longer times after train presentation (greater than 5 min), 2 cells out of 46 showed changes (increases) in synaptic efficacy in response to layer 1b stimulation. 4. In the current experiments both layers 1a and 1b showed statistically significant facilitation before the presentation of stimulus trains. However, layer 1b facilitation decreased from 22.7 +/- 3.5% to a statistically insignificant 3.9 +/- 3.3% after the presentation of trains, whereas layer 1a facilitation remained at a statistically significant level of 23.1 +/- 5.7%. 5. These experiments show that pyramidal cell responses to stimulation of the afferent and association fiber systems are affected differently by the previous presentation of trains of stimuli. This suggests that mechanisms of synaptic modification may differ between the afferent and intrinsic association synaptic projections onto single pyramidal cells in olfactory cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

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Deep neurons in piriform cortex. I. Morphology and synaptically evoked responses including a unique high-amplitude paired shock facilitation

Journal of Neurophysiology ◽

10.1152/jn.1989.62.2.369 ◽

1989 ◽

Vol 62 (2) ◽

pp. 369-385 ◽

Cited By ~ 53

Author(s):

G. F. Tseng ◽

L. B. Haberly

Keyword(s):

Lucifer Yellow ◽

Piriform Cortex ◽

Afferent Fiber ◽

Pyramidal Cells ◽

Excitatory Postsynaptic Potential ◽

Response Properties ◽

Postsynaptic Potential ◽

Association Fibers ◽

Axonal Arbors ◽

Stimulation Of

1. Synaptic responses of cells in layer III of the piriform cortex and the subjacent endopiriform nucleus (layer IV) were analyzed with intracellular recording techniques in a slice preparation from the rat, cut perpendicular to the pial surface. 2. Micropipettes containing Lucifer yellow (LY) were used to correlate response properties with morphology. An antiserum to LY was used to intensify staining and to prevent fading during detailed morphological study. Response properties were also examined with potassium acetate-containing electrodes. 3. Morphologically, two cell types were identified: pyramidal cells that were confined to layer III of the piriform cortex and multipolar cells that were in layer III and the endopiriform nucleus. 4. In morphology, deep pyramidal cells in layer III closely resembled superficial pyramidal cells in layer II, with the exception that primary apical dendritic trunks were longer and basal dendritic arborizations were more extensive than apical. Like superficial pyramidal cells, apical dendrites of all deep pyramidal cells stained extended through the afferent fiber termination zone in layer Ia and gave rise to local axonal arbors that were concentrated in layer III and the endopiriform nucleus. 5. Multipolar cells were morphologically indistinguishable in layer III and the endopiriform nucleus. All gave rise to nonvaricose spiny dendrites that never extended into layer II and local axonal arbors. 6. Response properties of deep pyramidal and multipolar cells were similar; responses of both of these populations were very different from those of superficial pyramidal cells. The primary difference between responses of deep pyramidal and multipolar cells was a shorter latency of postsynaptic potentials evoked in deep pyramidal cells by stimulation of afferent fibers, consistent with the extension of their dendrites into layer Ia. 7. Responses of most deep cells to stimulation of afferent and association fibers at sufficiently high strength consisted of an initial excitatory postsynaptic potential (EPSP), followed by a fast Cl- -mediated and a slow K+-mediated inhibitory postsynaptic potential (IPSP). 8. A characteristic feature of deep cells, which was only rarely observed in superficial pyramidal cells, was the presence of variable EPSPs evoked at long latencies (greater than 100 ms) by stimulation of afferent or association fibers. 9. A striking finding for deep pyramidal and multipolar cells, when studied with LY-containing pipettes, was a variable slowly rising depolarizing potential triggered at depolarized membrane potentials by stimulation of afferent or association fibers.(ABSTRACT TRUNCATED AT 400 WORDS)

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