Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex

Robert B. Levy, Alexander Reyes

Research output: Contribution to journalArticle

Abstract

The role of local cortical activity in shaping neuronal responses is controversial. Among other questions, it is unknown how the diverse response patterns reported in vivo-lateral inhibition in some cases, approximately balanced excitation and inhibition (co-tuning) in others-compare to the local spread of synaptic connectivity. Excitatory and inhibitory activity might cancel each other out, or, whether one outweighs the other, receptive field properties might be substantially affected. As a step toward addressing this question, we used multiple intracellular recording in mouse primary auditory cortical slices to map synaptic connectivity among excitatory pyramidal cells and the two broad classes of inhibitory cells, fast-spiking (FS) and non-FS cells in the principal input layer. Connection probability was distance-dependent; the spread of connectivity, parameterized by Gaussian fits to the data, was comparable for all cell types, ranging from 85 to 114 μm. With brief stimulus trains, unitary synapses formed by FS interneurons were stronger than other classes of synapses; synapse strength did not correlate with distance between cells. The physiological data were qualitatively consistent with predictions derived from anatomical reconstruction. We also analyzed the truncation of neuronal processes due to slicing; overall connectivity was reduced but the spatial pattern was unaffected. The comparable spatial patterns of connectivity and relatively strong excitatoryinhibitory interconnectivity are consistent with a theoretical model where either lateral inhibition or co-tuning can predominate, depending on the structure of the input.

Original languageEnglish (US)
Pages (from-to)5609-5619
Number of pages11
JournalJournal of Neuroscience
Volume32
Issue number16
DOIs
StatePublished - Apr 18 2012

Fingerprint

Auditory Cortex
Synapses
Pyramidal Cells
Interneurons
Theoretical Models

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex. / Levy, Robert B.; Reyes, Alexander.

In: Journal of Neuroscience, Vol. 32, No. 16, 18.04.2012, p. 5609-5619.

Research output: Contribution to journalArticle

@article{f737e55c00ac44e3a1c533f0a2625226,
title = "Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex",
abstract = "The role of local cortical activity in shaping neuronal responses is controversial. Among other questions, it is unknown how the diverse response patterns reported in vivo-lateral inhibition in some cases, approximately balanced excitation and inhibition (co-tuning) in others-compare to the local spread of synaptic connectivity. Excitatory and inhibitory activity might cancel each other out, or, whether one outweighs the other, receptive field properties might be substantially affected. As a step toward addressing this question, we used multiple intracellular recording in mouse primary auditory cortical slices to map synaptic connectivity among excitatory pyramidal cells and the two broad classes of inhibitory cells, fast-spiking (FS) and non-FS cells in the principal input layer. Connection probability was distance-dependent; the spread of connectivity, parameterized by Gaussian fits to the data, was comparable for all cell types, ranging from 85 to 114 μm. With brief stimulus trains, unitary synapses formed by FS interneurons were stronger than other classes of synapses; synapse strength did not correlate with distance between cells. The physiological data were qualitatively consistent with predictions derived from anatomical reconstruction. We also analyzed the truncation of neuronal processes due to slicing; overall connectivity was reduced but the spatial pattern was unaffected. The comparable spatial patterns of connectivity and relatively strong excitatoryinhibitory interconnectivity are consistent with a theoretical model where either lateral inhibition or co-tuning can predominate, depending on the structure of the input.",
author = "Levy, {Robert B.} and Alexander Reyes",
year = "2012",
month = "4",
day = "18",
doi = "10.1523/jneurosci.5158-11.2012",
language = "English (US)",
volume = "32",
pages = "5609--5619",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "16",

}

TY - JOUR

T1 - Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex

AU - Levy, Robert B.

AU - Reyes, Alexander

PY - 2012/4/18

Y1 - 2012/4/18

N2 - The role of local cortical activity in shaping neuronal responses is controversial. Among other questions, it is unknown how the diverse response patterns reported in vivo-lateral inhibition in some cases, approximately balanced excitation and inhibition (co-tuning) in others-compare to the local spread of synaptic connectivity. Excitatory and inhibitory activity might cancel each other out, or, whether one outweighs the other, receptive field properties might be substantially affected. As a step toward addressing this question, we used multiple intracellular recording in mouse primary auditory cortical slices to map synaptic connectivity among excitatory pyramidal cells and the two broad classes of inhibitory cells, fast-spiking (FS) and non-FS cells in the principal input layer. Connection probability was distance-dependent; the spread of connectivity, parameterized by Gaussian fits to the data, was comparable for all cell types, ranging from 85 to 114 μm. With brief stimulus trains, unitary synapses formed by FS interneurons were stronger than other classes of synapses; synapse strength did not correlate with distance between cells. The physiological data were qualitatively consistent with predictions derived from anatomical reconstruction. We also analyzed the truncation of neuronal processes due to slicing; overall connectivity was reduced but the spatial pattern was unaffected. The comparable spatial patterns of connectivity and relatively strong excitatoryinhibitory interconnectivity are consistent with a theoretical model where either lateral inhibition or co-tuning can predominate, depending on the structure of the input.

AB - The role of local cortical activity in shaping neuronal responses is controversial. Among other questions, it is unknown how the diverse response patterns reported in vivo-lateral inhibition in some cases, approximately balanced excitation and inhibition (co-tuning) in others-compare to the local spread of synaptic connectivity. Excitatory and inhibitory activity might cancel each other out, or, whether one outweighs the other, receptive field properties might be substantially affected. As a step toward addressing this question, we used multiple intracellular recording in mouse primary auditory cortical slices to map synaptic connectivity among excitatory pyramidal cells and the two broad classes of inhibitory cells, fast-spiking (FS) and non-FS cells in the principal input layer. Connection probability was distance-dependent; the spread of connectivity, parameterized by Gaussian fits to the data, was comparable for all cell types, ranging from 85 to 114 μm. With brief stimulus trains, unitary synapses formed by FS interneurons were stronger than other classes of synapses; synapse strength did not correlate with distance between cells. The physiological data were qualitatively consistent with predictions derived from anatomical reconstruction. We also analyzed the truncation of neuronal processes due to slicing; overall connectivity was reduced but the spatial pattern was unaffected. The comparable spatial patterns of connectivity and relatively strong excitatoryinhibitory interconnectivity are consistent with a theoretical model where either lateral inhibition or co-tuning can predominate, depending on the structure of the input.

UR - http://www.scopus.com/inward/record.url?scp=84859768155&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84859768155&partnerID=8YFLogxK

U2 - 10.1523/jneurosci.5158-11.2012

DO - 10.1523/jneurosci.5158-11.2012

M3 - Article

C2 - 22514322

AN - SCOPUS:84859768155

VL - 32

SP - 5609

EP - 5619

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 16

ER -