A hierarchical scheme proposed by Kaas and colleagues suggests that primate auditory cortex can be divided into core and belt regions based on anatomic connections with thalamus and distinctions among response properties. According to their model, core auditory cortex receives predominantly unimodal sensory input from the ventral nucleus of the medial geniculate body (MGBv); whereas belt cortex receives predominantly cross-modal sensory input from nuclei outside the MGBv. We previously characterized distinct response properties in rat primary (A1) versus ventral auditory field (VAF) cortex; however, it has been unclear whether VAF should be categorized as a core or belt auditory cortex. The current study employed high-resolution functional imaging to map intrinsic metabolic responses to tones and to guide retrograde tracer injections into A1 and VAF. The size and density of retrogradely labeled somas in the medial geniculate body (MGB) were examined as a function of their position along the caudal-to-rostral axis, subdivision of origin, and cortical projection target. A1 and VAF projecting neurons were found in the same subdivisions of the MGB but in rostral and caudal parts, respectively. Less than 3% of the cells projected to both regions. VAF projecting neurons were smaller than A1 projecting neurons located in dorsal (MGBd) and suprageniculate (SG) nuclei. Thus, soma size varied with both caudal-rostral position and cortical target. Finally, the majority (>70%) of A1 and VAF projecting neurons were located in MGBv. These MGB connection profiles suggest that rat auditory cortex, like primate auditory cortex, is made up of multiple distinct core regions.

A high-density, high-channel count, multiplexed ECoG array for auditory-cortex recordings.

Core auditory cortices are organized in parallel pathways that process incoming sensory information differently. In the rat, sound filtering properties of the primary (A1) and ventral (VAF) auditory fields are markedly different, yet both are core regions that by definition receive most of their thalamic input from the ventral nucleus (MGBv) of the medial geniculate body (MGB). For example, spike rate responses to sound intensity and frequency are more narrowly resolved in VAF vs. A1. Here we question whether there are anatomic correlates of the marked differences in response properties in these two core auditory fields. Combined Fourier optical imaging and multiunit recording methods were used to map tone frequency responses with high spatial resolution in A1, VAF, and neighboring cortices. The cortical distance representing a given octave was similar, yet response frequency resolution was about twice as large in VAF as in A1. Retrograde tracers were injected into low- and high-isofrequency contours of both regions to compare MGBv label patterns. The distance between clusters of MGBv neurons projecting to low- and high-isofrequency contours in the cortex was twice as large in caudal as in rostral MGB. This suggests that differences in A1 and VAF frequency resolution are related to the anatomic spatial resolution of frequency laminae in the thalamus, supporting a growing consensus that antecedents of cortical specialization can be attributed in part to the structural and functional characteristics of thalamocortical inputs.

A conserved feature of sound processing across species is the presence of multiple auditory cortical fields with topographically organized responses to sound frequency. Current organizational schemes propose that the ventral division of the medial geniculate body (MGBv) is a single functionally homogenous structure that provides the primary source of input to all neighboring frequency-organized cortical fields. These schemes fail to account for the contribution of MGBv to functional diversity between frequency-organized cortical fields. Here, we report response property differences for two auditory fields in the rat, and find they have nonoverlapping sources of thalamic input from the MGBv that are distinguished by the gene expression for type 1 vesicular glutamate transporter. These data challenge widely accepted organizational schemes and demonstrate a genetic plurality in the ascending glutamatergic pathways to frequency-organized auditory cortex.

Accurate orientation to sound under challenging conditions requires auditory cortex, but it is unclear how spatial attributes of the auditory scene are represented at this level. Current organization schemes follow a functional division whereby dorsal and ventral auditory cortices specialize to encode spatial and object features of sound source, respectively. However, few studies have examined spatial cue sensitivities in ventral cortices to support or reject such schemes. Here Fourier optical imaging was used to quantify best frequency responses and corresponding gradient organization in primary (A1), anterior, posterior, ventral (VAF), and suprarhinal (SRAF) auditory fields of the rat. Spike rate sensitivities to binaural interaural level difference (ILD) and average binaural level cues were probed in A1 and two ventral cortices, VAF and SRAF. Continuous distributions of best ILDs and ILD tuning metrics were observed in all cortices, suggesting this horizontal position cue is well covered. VAF and caudal SRAF in the right cerebral hemisphere responded maximally to midline horizontal position cues, whereas A1 and rostral SRAF responded maximally to ILD cues favoring more eccentric positions in the contralateral sound hemifield. SRAF had the highest incidence of binaural facilitation for ILD cues corresponding to midline positions, supporting current theories that auditory cortices have specialized and hierarchical functional organization.