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Spatial Organization of Frequency Response Areas and Rate/Level Functions in the Developing AI

¹Department of Otolaryngology—Head and Neck Surgery, and ²W. M. Keck Center for Integrative Neuroscience, University of California, San Francisco, California 94143; and ³Laboratoire Intégration de données multimédia, Unité Propre de Recherche de l'Enseignement Supérieur Equipe d'Accueil 3192, Faculté de Médecine, 35043 Rennes Cedex, France

Submitted 9 January 2003; accepted in final form 26 September 2003

The current study was conducted to extend our understanding of changes in spatial organization and response properties of cortical neurons in the developing mammalian forebrain. Extracellular multiunit responses to tones were recorded from a dense array of penetrations covering entire isofrequency contours in the primary auditory cortex (AI) of pentobarbital anesthetized kittens. Ages ranged from postnatal day 14 (P14), shortly after acquisition of normal auditory response thresholds, through postnatal day 111 (P111), when the kittens were largely mature. Spatial organization of the AI was tonotopically ordered by P14. The tonotopic gradient decreased with chronological maturation. At P14 the gradient was about 3.5 kHz/mm. By P111 it had declined to about 2.5 kHz/mm, so that the cortical region encompassing a fixed 3- to 15-kHz frequency range enlarged along its posterior-anterior dimension. Response properties of developing AI neurons changed in both frequency selectivity and intensity selectivity. The mean frequency tuning bandwidth increased with age. Initially, tuning bandwidths were narrow throughout the entire AI. With progressive maturation, broader bandwidths were observed in areas dorsal and ventral to a central region in which neurons remained narrowly tuned. The resulting spatial organization of tuning bandwidth was similar to that reported in adult cats. The majority of recording sites manifested nonmonotonic rate/level functions at all ages. However, the proportion of sites with monotonic rate/level functions increased with age. No spatial organization of rate/level functions (monotonic and nonmonotonic) was observed through P111. The relatively late development of bandwidth tuning in the AI compared with the early presence of tonotopic organization suggests that different developmental processes are responsible for structuring these two dimensions of acoustic selectivity.

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