Dendritic Compartment and Neuronal Output Mode Determine Pathway-Specific Long-Term Potentiation in the Piriform Cortex

Johenning, Friedrich W.; Beed, Prateep; Trimbuch, Thorsten; Bendels, M. H. K.; Winterer, Jochen; Schmitz, Dietmar

doi:10.1523/jneurosci.2672-09.2009

Cited by 44 publications

(64 citation statements)

References 51 publications

(87 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Experiments followed approved national and institutional guidelines for animal use. Acute slices of the aPC (400 m thickness) were prepared from Wistar rats of either sex (age, postnatal days 18 -25) in a coronal plane perpendicular to and containing the LOT (Johenning et al, 2009).…”

Section: Methodsmentioning

confidence: 99%

“…The stimulation electrode was placed in layer 1a, ventrally between the LOT and the imaged field of view (i.e., toward the LOT). Intracortical inputs were selectively blocked by 30 M baclofen (Tang and Hasselmo, 1994;Franks and Isaacson, 2005;Johenning et al, 2009). Stimulation strength was adjusted to be at the threshold for activation of at least one cell in the population with two stimuli.…”

Section: Methodsmentioning

confidence: 99%

“…We pharmacologically isolated this early, sensory component of aPC processing by selectively blocking associative fibers with baclofen (Tang and Hasselmo, 1994;Franks and Isaacson, 2005;Johenning et al, 2009). To compare the relative weight of sensory afferents within simultaneously stimulated populations of superficial and deep cells in aPC layer II, we used the multiple line scan technique (Lorincz et al, 2007) for fast two-photon population Ca 2ϩ imaging.…”

Section: Layer III Pyramidal Cells: Dorsoventral Asymmetry Of Recurrementioning

confidence: 99%

“…Recently, we demonstrated that bursting is a prerequisite for the induction of plasticity in associative layer 1b synapses (Johenning et al, 2009). aPC cells with high burst indices also display initial bursts firing at high frequencies (Suzuki and Bekkers, 2006).…”

Section: Implications For Cortical Odor Codingmentioning

confidence: 99%

See 3 more Smart Citations

Complementary Sensory and Associative Microcircuitry in Primary Olfactory Cortex

Wiegand¹,

Beed²,

Bendels³

et al. 2011

J. Neurosci.

Self Cite

View full text Add to dashboard Cite

The three-layered primary olfactory (piriform) cortex is the largest component of the olfactory cortex. Sensory and intracortical inputs converge on principal cells in the anterior piriform cortex (aPC). We characterize organization principles of the sensory and intracortical microcircuitry of layer II and III principal cells in acute slices of rat aPC using laser-scanning photostimulation and fast two-photon population Ca 2ϩ imaging. Layer II and III principal cells are set up on a superficial-to-deep vertical axis. We found that the position on this axis correlates with input resistance and bursting behavior. These parameters scale with distinct patterns of incorporation into sensory and associative microcircuits, resulting in a converse gradient of sensory and intracortical inputs. In layer II, sensory circuits dominate superficial cells, whereas incorporation in intracortical circuits increases with depth. Layer III pyramidal cells receive more intracortical inputs than layer II pyramidal cells, but with an asymmetric dorsal offset. This microcircuit organization results in a diverse hybrid feedforward/recurrent network of neurons integrating varying ratios of intracortical and sensory input depending on a cell's position on the superficial-to-deep vertical axis. Since burstiness of spiking correlates with both the cell's location on this axis and its incorporation in intracortical microcircuitry, the neuronal output mode may encode a given cell's involvement in sensory versus associative processing.

show abstract

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Layer III Pyramidal Cells: Dorsoventral Asymmetry Of Recurrementioning

confidence: 99%

Section: Implications For Cortical Odor Codingmentioning

confidence: 99%

See 2 more Smart Citations

Complementary Sensory and Associative Microcircuitry in Primary Olfactory Cortex

Wiegand¹,

Beed²,

Bendels³

et al. 2011

J. Neurosci.

Self Cite

View full text Add to dashboard Cite

show abstract

“…This approach has so far identified, for example, classes of glutamate-releasing principal neurons (Franks and Isaacson, 2006;Suzuki and Bekkers, 2006), their dendritic properties (Bathellier et al, 2009), circuits and synaptic plasticity (Franks and Isaacson, 2005;Poo and Isaacson, 2007;Johenning et al, 2009), and classes of GABA-releasing interneurons and their circuits (Young and Sun, 2009;Stokes and Isaacson, 2010;Suzuki and Bekkers, 2010a,b). We have previously reported that the main input layer of the PC, layer II, contains two functionally distinctive kinds of principal neurons, semilunar (SL) and superficial pyramidal (SP) cells (Suzuki and Bekkers, 2006).…”

Section: Introductionmentioning

confidence: 99%

Two Layers of Synaptic Processing by Principal Neurons in Piriform Cortex

Suzuki¹,

Bekkers²

2011

J. Neurosci.

166

View full text Add to dashboard Cite

The primary olfactory (or piriform) cortex is a trilaminar paleocortex that is thought to construct unified "odor images" from the odor components identified by the olfactory bulb. How the piriform cortex (PC) accomplishes this sophisticated synthetic task, despite its relatively simple architecture, is unknown. Here we used in vitro patch-clamp recordings from acute slices of the anterior PC of mice to identify microcircuits involved in excitatory synaptic processing. Cluster analysis confirmed the presence of two prominent classes of glutamatergic principal cells in the main input layer (layer II) of the PC: semilunar (SL) cells and superficial pyramidal (SP) cells. SL cells received stronger afferent excitatory input from the olfactory bulb, on average, than did SP cells. This was due to the larger mean strength of single-fiber afferents onto SL cells. In contrast, SP cells received stronger associational (intracortical) excitatory inputs, most likely due to their more extensive dendritic trees within the associational layers. Tissue-cut experiments and dual recordings from SL and SP cells in disinhibited slices were consistent with the distinctive patterns of connectivity of these two cell classes. Our findings suggest that the anterior PC employs at least two layers of excitatory synaptic processing: one involving strong afferent inputs onto SL cells, and another involving strong intracortical inputs onto SP cells. This architecture may allow the PC to sequentially process olfactory information within segregated subcircuits.

show abstract

GluK1 inhibits calcium dependent and independent transmitter release at associational/commissural synapses in area CA3 of the hippocampus

et al. 2010

View full text Add to dashboard Cite

CA3 pyramidal cells receive three main excitatory inputs: the first one is the mossy fiber input, synapsing mainly on the proximal apical dendrites. Second, entorhinal cortex cells form excitatory connections with CA3 pyramidal cells via the perforant path in the stratum lacunosum moleculare. The third input involves the ipsi-and contralateral connections, termed the associational/commissural (A/C) pathway terminating in the stratum radiatum of CA3, thus forming a feedback loop within this region. Since this excitatory recurrent synapse makes the CA3 region extremely prone to seizure development, understanding the regulation of synaptic strength of this connection is of crucial interest. Several studies suggest that kainate receptors (KAR) play a role in the regulation of synaptic strength. Our aim was to characterize the influence of KAR on A/C synaptic transmission: application of ATPA, a selective agonist of the GluK1 KAR, depressed the amplitude fEPSP without affecting the size of the fiber volley. Blockade of GABA receptors had no influence on this effect, arguing against the influence of interneuronal KARs. Pharmacological and genetic deletion studies could show that this effect was selectively due to GluK1 receptor activation. Several lines of evidence, such as PPF changes, coefficient of variance-analysis and glutamate uncaging experiments strongly argue for a presynaptic locus of suppression. This is accompanied by an ATPA-mediated reduction in Ca(2+) influx at excitatory synaptic terminals, which is most likely mediated by a G-Protein dependent mechanism, as suggested by application of pertussis toxin. Finally, analysis of miniature EPSCs in the presence and absence of extracellular Ca(2+) suggest that presynaptic KAR can also reduce transmitter release downstream and therefore independent of Ca(2+) influx.

show abstract

Dendritic Compartment and Neuronal Output Mode Determine Pathway-Specific Long-Term Potentiation in the Piriform Cortex

Cited by 44 publications

References 51 publications

Complementary Sensory and Associative Microcircuitry in Primary Olfactory Cortex

Complementary Sensory and Associative Microcircuitry in Primary Olfactory Cortex

Two Layers of Synaptic Processing by Principal Neurons in Piriform Cortex

GluK1 inhibits calcium dependent and independent transmitter release at associational/commissural synapses in area CA3 of the hippocampus

Contact Info

Product

Resources

About