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

Abstract

Auditory cortex neurons integrate information over a broad range of sound frequencies, yet it is not known how such integration is accomplished at the cellular or systems levels. Whereas information about frequencies near a neuron's characteristic frequency is likely to be relayed to the neuron by lemniscal thalamocortical inputs from the ventral division of the medial geniculate nucleus, we recently proposed that information about frequencies spectrally distant from characteristic frequency is mainly relayed to the neuron via "horizontal" intracortical projections from neurons with spectrally-distant characteristic frequencies [J Neurophysiol 91 (2004) 2551]. Here we test this hypothesis by using current source density analysis to determine if characteristic frequency and spectrally-distant non-characteristic frequency stimuli preferentially activate thalamocortical and horizontal pathways, respectively, in rat auditory cortex. Characteristic frequency stimuli produced current source density profiles with prominent initial current sinks in layers 3 and 4--the termination zone of lemniscal inputs from medial geniculate nucleus. In contrast, stimuli three octaves below characteristic frequency produced initial current sinks mainly in the infragranular layers. Differences between current source density profiles were only apparent for initial current sinks; profiles for longer-latency current sinks evoked by characteristic frequency and non-characteristic frequency stimuli overlapped to a greater degree, likely due to shared mechanisms of intracortical processing or to longer-latency thalamocortical contributions (lemniscal and nonlemniscal). To identify current source density profiles produced by activation of lemniscal thalamocortical inputs alone, we utilized the mouse auditory thalamocortical slice preparation. Electrical stimulation of the medial geniculate nucleus in vitro produced major current sinks in cortical layers 3/4, and excitation spread horizontally from this point throughout primary auditory cortex to produce current sinks in multiple cortical layers. These data support the hypothesis that relay of thalamocortical information throughout auditory cortex via horizontal intracortical projections may be the basis of broad spectral integration in vivo.