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The Journal of Neuroscience, August 13, 2008, 28(33):8273-8284; doi:10.1523/JNEUROSCI.5701-07.2008

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Cellular/Molecular
Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex

Moritz Helmstaedter,1 Jochen F. Staiger,2 Bert Sakmann,1 and Dirk Feldmeyer3,4

1Max Planck Institute for Medical Research, D-69120 Heidelberg, Germany, 2Department of Neuroanatomy, Institute for Anatomy and Cell Biology, Albert-Ludwigs-Universität, D-79104 Freiburg, Germany, and 3Research Center Jülich, Institute for Neuroscience and Biophysics, INB-3 Medicine, D-52425 Jülich, Germany, and 4Department of Psychiatry and Psychotherapy, RWTH Aachen University Hospital, D-52074 Aachen, Germany

Correspondence should be addressed to Moritz Helmstaedter, Max Planck Institute for Medical Research, Jahnstrasse 29, D-69120 Heidelberg, Germany. Email: moritz.helmstaedter{at}mpimf-heidelberg.mpg.de

Interneurons in layers 2/3 are excited by pyramidal cells within the same layer (Reyes et al., 1998; Gupta et al., 2000), but little is known about translaminar innervation of these interneurons by spiny neurons in the main cortical input layer 4 (L4). Here, we investigated (1) how efficiently L4 spiny neurons excite L2/3 interneurons via monosynaptic connections, (2) whether glutamate release from axon terminals of L4 spiny neurons depends on the identity of the postsynaptic interneuron, and (3) how L4-to-L2/3 interneuron connections compare with L4-to-L2/3 pyramidal neuron connections. We recorded from pairs of L4 spiny neurons and L2/3 interneurons in acute slices of rat barrel cortex of postnatal day 20 (P20) to P29 rats. The L4-to-L2/3 interneuron connections had an average unitary EPSP of 1.2 ± 1.1 mV. We found an average of 2.3 ± 0.8 contacts per connection, and the L4-to-L2/3 interneuron innervation domains were mostly column restricted. Unitary EPSP amplitudes and paired-pulse ratios in the L4-to-L2/3 interneuron connections depended on the "group" of the postsynaptic interneuron. Averaged over all L4-to-L2/3 interneuron connections, unitary EPSP amplitudes were 1.8-fold higher than in the translaminar L4-to-L2/3 pyramidal cell connections. Our results suggest that L4 spiny neurons may more efficiently recruit L2/3 interneurons than L2/3 pyramidal neurons, and that glutamate release from translaminar boutons of L4 spiny neuron axons is target cell specific.

Key words: barrel cortex; connectivity; GABAergic interneurons; layer 2/3; synaptic connection; target cell specificity


Received Dec. 22, 2007; revised May 26, 2008; accepted June 19, 2008.

Correspondence should be addressed to Moritz Helmstaedter, Max Planck Institute for Medical Research, Jahnstrasse 29, D-69120 Heidelberg, Germany. Email: moritz.helmstaedter{at}mpimf-heidelberg.mpg.de




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