Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys

Abstract

Microelectrode recordings were used to investigate the tonotopic organization of auditory cortex of macaque monkeys and guide the placement of injections of wheat germ agglutinin-horse radish peroxidase (WGA-HRP) and fluorescent dyes. Anatomical and physiological results were later related to histological distinctions in the same brains after sections were processed for cytoarchitecture, myeloarchitecture, acetylcholinesterase (AchE), or cytochrome oxidase (CO). The experiments produced several major findings. (1) Neurons throughout a broad expanse of cortex were highly responsive to pure tones, and best frequencies could be determined for neurons in arrays of recording sites. (2) The microelectrode recordings revealed two systematic representations of tone frequencies, the primary area (AI) and a primary-like rostral field (R) as previously described. The representation of high to low frequency tones in A1 was largely caudorostral along the plane of the sulcus. A reversal of the order of representation of frequencies occurred in R. (3) AI and R together were coextensive with a koniocellular, densely myelinated zone that expressed high levels of AchE and CO. These architectonic features were somewhat less pronounced in R than AI, but a clear border between the two areas was not apparent. (4) Cortex bordering AI and R was less responsive to tones, but when best frequencies for neurons could be determined, they matched those for adjoining parts of AI and R. (5) Architectonically distinct regions were apparent within some of the cortex bordering AI and R. (6) The major ipsilateral cortical connections of AI were with R and cortex immediately lateral and medial to AI. (7) Callosal connections of AI were predominantly with matched locations in the opposite AI, but they also included adjoining fields. (8) Neurons in the ventral (MGV), medial (MGM), and dorsal (MGD) nuclei of the medial geniculate complex projected to AI and cortex lateral to AI. (9) Injections in cortex responsive to high frequency tones labeled more dorsal parts of MGV than injections in cortex responsive to low frequency tones.

Orthogonal acoustic dimensions define auditory field maps in human cortex

“…It is likely that the AFMs surrounding the HG cluster are also roughly half of two additional clover leaf clusters, based on the prevalence of this type of organization in VFMs (4,6,7,(35)(36)(37)40). Our results are consistent with predictions from the widely accepted macaque model of auditory core and belt, based on measurements of tonotopy, periodicity, cytoarchitecture, and connectivity (10)(11)(12)(13)(14)(15)(16)(17)(18). The present results are also consistent with the published data, although not necessarily the interpretation, of previous studies of tonotopic gradients in humans (23)(24)(25)(26)(27)(28).…”

“…In audition, there has been only one dimension of sensory topography clearly mapped in cortex, which makes it impossible to use sensory topography to accurately differentiate specific human cortical auditory field maps (AFMs). Current estimates of human AFMs rely primarily on a monkey model that is well characterized by cytoarchitectonics (10,11), single-and multiunit physiology (12)(13)(14)(15)(16), tracer studies (17), and functional magnetic resonance imaging (fMRI) (18). Human cytoarchitectonic measurements generally resemble those in macaque monkey and indicate that the small subfields of primary auditory cortex are confined to Heschl's gyrus (HG; or between HG-1 and HG-2, in cases where a double gyrus exists) and oriented medial to lateral along HG (19)(20)(21)(22).…”

Human Primary Auditory Cortex Follows the Shape of Heschl's Gyrus

“…5 D, E), resulting in compact cortical wiring. Indeed, monkey AI and R are highly interconnected between matching tonotopic locations (Morel and Kaas, 1992;Morel et al, 1993). While this hypothesis could explain the emergence of HG, it would not explain the variable existence of the SI.…”

“…The neurons of each field respond to tones over a limited frequency range and are spatially arranged according to preferred frequencies-tonotopy (Brugge and Merzenich, 1973;Morel et al, 1993;Kaas and Hackett, 2000). Along a posterior-to-anterior axis, there is a continuous mapping of preferred frequencies from high to low (A1), followed by a reversed mapping of low back to high (R), followed by a third smaller mapping of high back to low (RT).…”

Consequences of unilateral hearing loss: Cortical adjustment to unilateral deprivation

“…Until recently, AI and AAF were considered to be, in essence, mirror images of one another, each possessing a strict and orderly tonotopic map (e.g., Merzenich et al, 1975;Knight 1977;Imig, 1980, Phillips andIrvine, 1982;Morel et al, 1993;Thomas et al, 1993;Stiebler et al, 1997;Rutkowski et al, 2003) and having similar anatomical connections (e.g., Anderson et al, 1980b;Imig and Reale, 1980;Imig and Morel, 1983), though AAF occupies a smaller area of cortex. This concept has been challenged in several species, based on anatomical, behavioral, and physiological evidence.…”