Subdivisions and connections of auditory cortex in owl monkeys

Abstract

The organization and connections of auditory cortex in owl monkeys, Aotus trivirgatus, were investigated by combining microelectrode mapping methods with studies of architecture and connections in the same animals. In most experiments, portions of auditory cortex were first explored with microelectrodes, neurons were characterized as responsive or not to auditory stimuli, and best frequencies were determined whenever possible. Most recordings were in cortex previously designated as primary (A‐I) and rostral (R) auditory fields (Imig et al. J Comp Neurol 171:111, '77) and in a newly defined rostrotemporal field (RT) located rostral to R. Injections of wheat germ agglutinin‐horseradish peroxidase (WGAx‐HRP) and fluorescent tracers were placed in electrophysiologically identified locations of Ax‐I, R, and RT; the posterolateral (PL) and anterolateral (AL) divisions of a narrow belt of auditory cortex lateral and adjacent to Ax‐I and R; cortex of the superior temporal gyrus lateral and rostrolateral to PL and AL; and regions of prefrontal cortex that receive inputs from auditory cortex. There were several major findings: 1. Best frequencies were most clearly determined for neurons within a densely myelinated strip of cortex on the lower bank and lip of the lateral sulcus. We divided this strip into three fields, A‐I, R, and RT, although an alternative interpretation that A‐I and R are parts of a single field remains tenable. In some cases, isofrequency contours appeared to continue uninterrupted across fields Ax‐I and R, with lower frequencies represented laterally and higher frequencies represented deeper in the sulcus. In other cases, there was a tendency for high frequencies to be represented caudally and medially, and low frequencies laterally in Ax‐I and rostrally in R, with partial discontinuity in the isofrequency contours. A reversal of the tonotopic gradient appeared in RT with a common lowx‐frequency representation at the caudal border with R, and progressively higher frequencies encountered rostrally. Of the three fields, Ax‐I appears slightly more myelinated than R, and RT slightly less than R. The distinctiveness of the three fields is further demonstrated by the patterns of connections. In particular, Ax‐I and RT are both interconnected with R, but not with each other. Connections between Ax‐I and R are between tonotopically matched locations. 2. A narrow 2–3 mm wide band of cortex lateral to A‐I, R, and RT was also responsive to auditory stimuli, but typically neurons were more difficult to activate, and best frequencies were more difficult to determine. No distinctions in myeloarchitecture or CO activity were obvious. Nevertheless, regions roughly corresponding to previously distinguished PL and AL divisions of the belt cortex (Imig et al. J Comp Neurol 171:111, '77) were interconnected. Both PL and AL were connected with R, but PL was connected with A‐I while AL was connected with RT. We also denoted a lateral rostrotemporal zone lateral to RT, with inputs from R, RT, and cortex rostral to RT. 3. Another proposed subdivision is CM, a moderately myelinated area medial to A‐I that is somewhat smaller than the CM of Imig et al. ('77). CM has connections with A‐I, R, PL, and AL. Other parts of the caudal, medial, and rostral belt cortex have auditory connections either from the core areas or other parts of the belt, so that overall there appear to be seven or more fields, but the exact number and boundaries remain uncertain. 4. Patterns of connections also implicate cortex lateral and laterorostral to the belt in auditory function. Cortex lateral to PL interconnects with PL and cortex lateral to AL, and this cortex and the cortex lateral and rostral to the belt have inputs from the auditory thalamus. 5. PL, AL and cortex lateral to these fields connect with cortex rostromedial to the frontal eye field. A‐I, R, and RT do not directly connect with prefrontal cortex. 6. In the thalamus, the ventral division of the medial geniculate complex (MGV) projects to A‐I, R, RT, and possibly weakly to PL and AL. The projections to different tonotopic locations in A‐I and R suggest that low frequencies are represented caudoventrally and high frequencies rostrodorsally in MGV. The medial or magnocellular division (MGM) has more widespread projections to auditory cortex, including A‐I, R, AL, and the lateral rostral temporal area (LRT). Although less precise than those of MGV, projections to A‐I from MGM tend to be topographically organized with neurons projecting to high‐frequency targets distributed dorsal to neurons projecting to low‐frequency targets. The dorsal division, MGD, projects to R, RT, AL, and LRT, with more rostral fields receiving projections from the more caudal regions of MGD. The suprageniculate and limitans nuclei, as well as the medial pulvinar, also contribute to auditory fields outside the core areas A‐I, R, and RT. 7. A‐I, R, and RT project to the central nucleus of the inferior colliculus (CN), with A‐I projections extending into the laminated portion of the CN. Other parts of the auditory cortex, including AL. and rostrolateral temporal cortex, project to the dorsal cortex (DC) and external nucleus (EN).