Optogenetic Mapping of Intracortical Circuits Originating from Semilunar Cells in the Piriform Cortex

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2015 Oct 28

PMID 26503263

Citations 17

Authors

Julian M C Choy

Norimitsu Suzuki

Yasuyuki Shima

Timotheus Budisantoso

Sacha B Nelson

John M Bekkers

Affiliations

Soon will be listed here.

Abstract

Despite its comparatively simple trilaminar architecture, the primary olfactory (piriform) cortex of mammals is capable of performing sophisticated sensory processing, an ability that is thought to depend critically on its extensive associational (intracortical) excitatory circuits. Here, we used a novel transgenic mouse model and optogenetics to measure the connectivity of associational circuits that originate in semilunar (SL) cells in layer 2a of the anterior piriform cortex (aPC). We generated a mouse line (48L) in which channelrhodopsin-2 (ChR) could be selectively expressed in a subset of SL cells. Light-evoked excitatory postsynaptic currents (EPSCs) could be evoked in superficial pyramidal cells (17.4% of n = 86 neurons) and deep pyramidal cells (33.3%, n = 9) in the aPC, but never in ChR- SL cells (0%, n = 34). Thus, SL cells monosynaptically excite pyramidal cells, but not other SL cells. Light-evoked EPSCs were also selectively elicited in 3 classes of GABAergic interneurons in layer 3 of the aPC. Our results show that SL cells are specialized for providing feedforward excitation of specific classes of neurons in the aPC, confirming that SL cells comprise a functionally distinctive input layer.

Citing Articles

Lateral entorhinal cortex afferents reconfigure the activity in piriform cortex circuits.

Pedroncini O, Federman N, Marin-Burgin A Proc Natl Acad Sci U S A. 2024; 121(48):e2414038121.

PMID: 39570314 PMC: 11621770. DOI: 10.1073/pnas.2414038121.

Lateral lamina V projection neuron axon collaterals connect sensory processing across the dorsal horn of the mouse spinal cord.

Browne T, Smith K, Gradwell M, Dayas C, Callister R, Hughes D Sci Rep. 2024; 14(1):26354.

PMID: 39487174 PMC: 11530558. DOI: 10.1038/s41598-024-73620-4.

Parallel processing by distinct classes of principal neurons in the olfactory cortex.

Nagappan S, Franks K Elife. 2021; 10.

PMID: 34913870 PMC: 8676325. DOI: 10.7554/eLife.73668.

Olfactory Optogenetics: Light Illuminates the Chemical Sensing Mechanisms of Biological Olfactory Systems.

Zhu P, Tian Y, Chen Y, Chen W, Wang P, Du L Biosensors (Basel). 2021; 11(9).

PMID: 34562900 PMC: 8470751. DOI: 10.3390/bios11090309.

Chronic loss of inhibition in piriform cortex following brief, daily optogenetic stimulation.

Ryu B, Nagappan S, Santos-Valencia F, Lee P, Rodriguez E, Lackie M Cell Rep. 2021; 35(3):109001.

PMID: 33882304 PMC: 8102022. DOI: 10.1016/j.celrep.2021.109001.

References

Hagiwara A, Pal S, Sato T, Wienisch M, Murthy V . Optophysiological analysis of associational circuits in the olfactory cortex. Front Neural Circuits. 2012; 6:18. PMC: 3329886. DOI: 10.3389/fncir.2012.00018. View

Tantirigama M, Oswald M, Duynstee C, Hughes S, Empson R . Expression of the developmental transcription factor Fezf2 identifies a distinct subpopulation of layer 5 intratelencephalic-projection neurons in mature mouse motor cortex. J Neurosci. 2014; 34(12):4303-8. PMC: 6608095. DOI: 10.1523/JNEUROSCI.3111-13.2014. View

Suzuki N, Bekkers J . Neural coding by two classes of principal cells in the mouse piriform cortex. J Neurosci. 2006; 26(46):11938-47. PMC: 6674875. DOI: 10.1523/JNEUROSCI.3473-06.2006. View

Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T . Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol. 2003; 467(1):60-79. DOI: 10.1002/cne.10905. View

Sugino K, Hempel C, Miller M, Hattox A, Shapiro P, Wu C . Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci. 2005; 9(1):99-107. DOI: 10.1038/nn1618. View

Franks K, Isaacson J . Synapse-specific downregulation of NMDA receptors by early experience: a critical period for plasticity of sensory input to olfactory cortex. Neuron. 2005; 47(1):101-14. DOI: 10.1016/j.neuron.2005.05.024. View

Haberly L, Bower J . Olfactory cortex: model circuit for study of associative memory?. Trends Neurosci. 1989; 12(7):258-64. DOI: 10.1016/0166-2236(89)90025-8. View

de Almeida L, Idiart M, Linster C . A model of cholinergic modulation in olfactory bulb and piriform cortex. J Neurophysiol. 2012; 109(5):1360-77. PMC: 3602836. DOI: 10.1152/jn.00577.2012. View

Luna V, Morozov A . Input-specific excitation of olfactory cortex microcircuits. Front Neural Circuits. 2012; 6:69. PMC: 3446699. DOI: 10.3389/fncir.2012.00069. View

10.

Haberly L, Price J . Association and commissural fiber systems of the olfactory cortex of the rat. J Comp Neurol. 1978; 178(4):711-40. DOI: 10.1002/cne.901780408. View

11.

Hasselmo M, Barkai E . Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J Neurosci. 1995; 15(10):6592-604. PMC: 6577978. View

12.

Petreanu L, Huber D, Sobczyk A, Svoboda K . Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci. 2007; 10(5):663-8. DOI: 10.1038/nn1891. View

13.

Haberly L, Bower J . Analysis of association fiber system in piriform cortex with intracellular recording and staining techniques. J Neurophysiol. 1984; 51(1):90-112. DOI: 10.1152/jn.1984.51.1.90. View

14.

Hopfield J . Pattern recognition computation using action potential timing for stimulus representation. Nature. 1995; 376(6535):33-6. DOI: 10.1038/376033a0. View

15.

Treves A, Rolls E . Computational analysis of the role of the hippocampus in memory. Hippocampus. 1994; 4(3):374-91. DOI: 10.1002/hipo.450040319. View

16.

Bekkers J, Suzuki N . Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci. 2013; 36(7):429-38. DOI: 10.1016/j.tins.2013.04.005. View

17.

Quattrocolo G, Maccaferri G . Optogenetic activation of cajal-retzius cells reveals their glutamatergic output and a novel feedforward circuit in the developing mouse hippocampus. J Neurosci. 2014; 34(39):13018-32. PMC: 4172799. DOI: 10.1523/JNEUROSCI.1407-14.2014. View

18.

Petreanu L, Mao T, Sternson S, Svoboda K . The subcellular organization of neocortical excitatory connections. Nature. 2009; 457(7233):1142-5. PMC: 2745650. DOI: 10.1038/nature07709. View

19.

Haberly L . Structure of the piriform cortex of the opossum. I. Description of neuron types with Golgi methods. J Comp Neurol. 1983; 213(2):163-87. DOI: 10.1002/cne.902130205. View

20.

Franks K, Russo M, Sosulski D, Mulligan A, Siegelbaum S, Axel R . Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron. 2011; 72(1):49-56. PMC: 3219421. DOI: 10.1016/j.neuron.2011.08.020. View