Spectral integration in primary auditory cortex: Laminar processing of afferent input, in vivo and in vitro

Kaur, Simranjit; Rose, Heather J.; Lazar, Ronit; Liang, Kevin; Metherate, Raju

doi:10.1016/j.neuroscience.2005.04.052

Cited by 107 publications

(115 citation statements)

References 53 publications

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“…The observed CSD patterns are in agreement with previous accounts of the order of activation in the rodent primary auditory cortex, in which responses with very short latency are found not only in the chief thalamo-recipient layers in auditory cortex (lower layer III and layer IV; Smith and Populin, 2001) but also in the deepest cortical layers. This has been observed in rats (Kaur et al, 2005;Szymanski et al, 2009), mice (Shen et al, 1999), gerbils (Sugimoto et al, 1997), and guinea pigs (Wallace and Palmer, 2008). The neural activity triggered by the afferent input, near 500 m (deep layer III and layer IV), then spreads upward to supragranular layers, as well as downward to infragranular layers.…”

Section: Lfp and Csd Responses To Tonal Stimulationmentioning

confidence: 79%

The Laminar and Temporal Structure of Stimulus Information in the Phase of Field Potentials of Auditory Cortex

et al. 2011

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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.

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Section: Lfp and Csd Responses To Tonal Stimulationmentioning

confidence: 79%

The Laminar and Temporal Structure of Stimulus Information in the Phase of Field Potentials of Auditory Cortex

et al. 2011

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“…4). The absent FRA edges are usually driven primarily by CC connectivity (42)(43)(44). Therefore, we propose that the decrease in receptive field size may be a change related to a decreased ability of CC connections to drive responses.…”

Section: Discussionmentioning

confidence: 89%

Chronic reduction in inhibition reduces receptive field size in mouse auditory cortex

Seybold

Stanco

Cho³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Inhibitory interneurons regulate the responses of cortical circuits. In auditory cortical areas, inhibition from these neurons narrows spectral tuning and shapes response dynamics. Acute disruptions of inhibition expand spectral receptive fields. However, the effects of long-term perturbations of inhibitory circuitry on auditory cortical responses are unknown. We ablated ∼30% of dendrite-targeting cortical inhibitory interneurons after the critical period by studying mice with a conditional deletion of Dlx1. Following the loss of interneurons, baseline firing rates rose and tone-evoked responses became less sparse in auditory cortex. However, contrary to acute blockades of inhibition, the sizes of spectral receptive fields were reduced, demonstrating both higher thresholds and narrower bandwidths. Furthermore, long-latency responses at the edge of the receptive field were absent. On the basis of changes in response dynamics, the mechanism for the reduction in receptive field size appears to be a compensatory loss of corticocortically (CC) driven responses. Our findings suggest chronic conditions that feature changes in inhibitory circuitry are not likely to be well modeled by acute network manipulations, and compensation may be a critical component of chronic neuronal conditions. P rocessing of auditory information in the auditory cortex underlies the conscious perception of sound and speech comprehension. Inhibitory interneurons, representing ∼20% of cortical neurons (1), regulate this processing by shaping the spectral tuning (2-13), temporal tuning (14-16), and response dynamics of local excitatory neurons (5-11). Inhibitory interneurons form multiple subtypes on the basis of morphology, physiology, and biochemistry (1, 17) that likely serve distinct roles in cortical processing.Loss of inhibitory interneurons is observed in conditions that affect cortical processing in humans, and in animal models of human disorders, including aging (18, 19), autism (20), schizophrenia (21-23), traumatic brain injury (TBI) (24), hearing loss (25-28), and tinnitus (29). Often, a particular disease is associated with a specific deficit in a subset of interneurons. For example, rodent models of autism demonstrate a loss of parvalbumin positive (PV + ) interneurons (20), whereas aging and TBI models show a greater loss of somatostatin (SST) + interneurons than other interneuron populations (19,24). The disruption of specific interneuron populations may underlie the particular cognitive defects associated with each condition. Therefore, it is necessary to understand the effects following chronic reductions of particular interneuron subtypes.One mouse model of an adult-onset loss of dendrite-targeting interneurons (DTIs) is the Dlx1 mutant (30). Dlx1 encodes a homeobox transcription factor from the Dlx family that regulates the development, migration, and survival of cortical interneurons (30-32). In Dlx1 mutants, the other Dlx family members compensate for the deficiency and thereby allow interneurons to migrate into cortex (30)....

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“…We quantified changes of the laminar CSD profile after cortical silencing, which allows insights into the relative contributions, the temporal recruitment, and the laminar organization of afferent thalamocortical input and intracortical input, respectively, to primary auditory cortex (cf. Schroeder et al, 2003;Kaur et al, 2005;Lakatos et al, 2005Lakatos et al, , 2007Chen et al, 2007).…”

Section: Resultsmentioning

confidence: 99%

Spectral Integration in Primary Auditory Cortex Attributable to Temporally Precise Convergence of Thalamocortical and Intracortical Input

Happel¹,

Jeschke²,

Ohl³

2010

J. Neurosci.

130

276

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Primary sensory cortex integrates sensory information from afferent feedforward thalamocortical projection systems and convergent intracortical microcircuits. Both input systems have been demonstrated to provide different aspects of sensory information. Here we have used high-density recordings of laminar current source density (CSD) distributions in primary auditory cortex of Mongolian gerbils in combination with pharmacological silencing of cortical activity and analysis of the residual CSD, to dissociate the feedforward thalamocortical contribution and the intracortical contribution to spectral integration. We found a temporally highly precise integration of both types of inputs when the stimulation frequency was in close spectral neighborhood of the best frequency of the measurement site, in which the overlap between both inputs is maximal. Local intracortical connections provide both directly feedforward excitatory and modulatory input from adjacent cortical sites, which determine how concurrent afferent inputs are integrated. Through separate excitatory horizontal projections, terminating in cortical layers II/III, information about stimulus energy in greater spectral distance is provided even over long cortical distances. These projections effectively broaden spectral tuning width. Based on these data, we suggest a mechanism of spectral integration in primary auditory cortex that is based on temporally precise interactions of afferent thalamocortical inputs and different short-and long-range intracortical networks. The proposed conceptual framework allows integration of different and partly controversial anatomical and physiological models of spectral integration in the literature.

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Spectral integration in primary auditory cortex: Laminar processing of afferent input, in vivo and in vitro

Cited by 107 publications

References 53 publications

The Laminar and Temporal Structure of Stimulus Information in the Phase of Field Potentials of Auditory Cortex

The Laminar and Temporal Structure of Stimulus Information in the Phase of Field Potentials of Auditory Cortex

Chronic reduction in inhibition reduces receptive field size in mouse auditory cortex

Spectral Integration in Primary Auditory Cortex Attributable to Temporally Precise Convergence of Thalamocortical and Intracortical Input

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