The laminar and temporal structure of stimulus information in the phase of field potentials of auditory cortex

TY - JOUR

T1 - The laminar and temporal structure of stimulus information in the phase of field potentials of auditory cortex

AU - Szymanski, Francois D

AU - Rabinowitz, Neil C

AU - Magri, Cesare

AU - Panzeri, Stefano

AU - Schnupp, Jan W H

PY - 2011/11/2

Y1 - 2011/11/2

N2 - Recent studies have shown that the phase of low-frequency local field potentials (LFPs) in sensory cortices carries a significant amount of information about complex naturalistic stimuli, yet the laminar circuit mechanisms and the aspects of stimulus dynamics responsible for generating this phase information remain essentially unknown. Here we investigated these issues by means of an information theoretic analysis of LFPs and current source densities (CSDs) recorded with laminar multi-electrode arrays in the primary auditory area of anesthetized rats during complex acoustic stimulation (music and broadband 1/f stimuli). We found that most LFP phase information originated from discrete "CSD events" consisting of granular-superficial layer dipoles of short duration and large amplitude, which we hypothesize to be triggered by transient thalamocortical activation. These CSD events occurred at rates of 2-4 Hz during both stimulation with complex sounds and silence. During stimulation with complex sounds, these events reliably reset the LFP phases at specific times during the stimulation history. These facts suggest that the informativeness of LFP phase in rat auditory cortex is the result of transient, large-amplitude events, of the "evoked" or "driving" type, reflecting strong depolarization in thalamo-recipient layers of cortex. Finally, the CSD events were characterized by a small number of discrete types of infragranular activation. The extent to which infragranular regions were activated was stimulus dependent. These patterns of infragranular activations may reflect a categorical evaluation of stimulus episodes by the local circuit to determine whether to pass on stimulus information through the output layers.

AB - Recent studies have shown that the phase of low-frequency local field potentials (LFPs) in sensory cortices carries a significant amount of information about complex naturalistic stimuli, yet the laminar circuit mechanisms and the aspects of stimulus dynamics responsible for generating this phase information remain essentially unknown. Here we investigated these issues by means of an information theoretic analysis of LFPs and current source densities (CSDs) recorded with laminar multi-electrode arrays in the primary auditory area of anesthetized rats during complex acoustic stimulation (music and broadband 1/f stimuli). We found that most LFP phase information originated from discrete "CSD events" consisting of granular-superficial layer dipoles of short duration and large amplitude, which we hypothesize to be triggered by transient thalamocortical activation. These CSD events occurred at rates of 2-4 Hz during both stimulation with complex sounds and silence. During stimulation with complex sounds, these events reliably reset the LFP phases at specific times during the stimulation history. These facts suggest that the informativeness of LFP phase in rat auditory cortex is the result of transient, large-amplitude events, of the "evoked" or "driving" type, reflecting strong depolarization in thalamo-recipient layers of cortex. Finally, the CSD events were characterized by a small number of discrete types of infragranular activation. The extent to which infragranular regions were activated was stimulus dependent. These patterns of infragranular activations may reflect a categorical evaluation of stimulus episodes by the local circuit to determine whether to pass on stimulus information through the output layers.

KW - Acoustic Stimulation

KW - Animals

KW - Auditory Cortex/physiology

KW - Auditory Pathways/physiology

KW - Brain Mapping

KW - Data Interpretation, Statistical

KW - Electrophysiology

KW - Evoked Potentials, Auditory/physiology

KW - Female

KW - Rats

KW - Rats, Long-Evans

KW - Signal Processing, Computer-Assisted

KW - Spectrum Analysis

U2 - 10.1523/JNEUROSCI.1416-11.2011

DO - 10.1523/JNEUROSCI.1416-11.2011

M3 - SCORING: Journal article

C2 - 22049422

VL - 31

SP - 15787

EP - 15801

JO - J NEUROSCI

JF - J NEUROSCI

SN - 0270-6474

IS - 44

ER -