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

Abstract

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.

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

“…The response latency of control units is longer at low intensities near threshold compared with high intensities (medians: CT-high = 15.5 ms, CT-low = 22 ms, Bonferroni corrected P < 0.001, Fig. 3G) in agreement with previous results where CC driven responses have longer latencies (44,45). However, in cKO units, the response latency at low intensities occurs significantly earlier than in control units (medians: CT-low = 22 ms, cKO-low = 16 ms, Bonferroni corrected P < 0.05, Fig.…”

“…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.…”

“…Thus, the changes observed in cortex were not present in the thalamus-the preceding subcortical station-and likely arise in cortex. processes and horizontal cortical spread of activity (44,45). Therefore, we measured the response dynamics at the center and edge of the FRA to explore how effectively CC connections drive activity in cKO mutants.…”

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

“…The events were defined by a strong granular layer activation, characterized by brief (ϳ50 ms), large-amplitude current sinks in thalamo-recipient layers and current sources in superficial layers. This suggests that they reflect mostly bursts of thalamocortical activation, although it is conceivable that they may also reflect some corticocortical activation (Happel et al, 2010). Although such CSD events could occur spontaneously, in the presence of stimulation, they were nevertheless stimulus tuned.…”

Dopamine-Modulated Recurrent Corticoefferent Feedback in Primary Sensory Cortex Promotes Detection of Behaviorally Relevant Stimuli

“…By exploiting a previously established technique to dissociate intracortically relayed components from thalamocortically relayed components of cortical stimulus-induced excitation (Happel et al, 2010), we investigated the effects of dopaminergic neuromodulation in primary auditory cortex (AI) of Mongolian gerbils on a systems level. In a stepwise approach of circuit analysis, using auditory stimulation, layer-specific intracortical microstimulation (ICMS), laminar current-source-density (CSD) analysis (Mitzdorf, 1985;Happel et al, 2010), pharmacological manipulation, and behavioral analysis ( Fig.…”