, Volume 102, Issue 2, pp 210-226

Level-dependent representation of stimulus frequency in cat primary auditory cortex

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Abstract

The tonotopicity of the cat's primary auditory cortex (AI) is thought to provide the framework for frequency-specific processing in that field. This study was designed to assess this postulate by examining the spatial distribution of neurons within AI that are activated by a single tonal frequency delivered to the contralateral ear. Distributions obtained at each of several stimulus levels were then compared to assess the influence of stimulus amplitude on the spatial representation of a given stimulus frequency in AI. Data were obtained from 308 single units in AI of four adult, barbiturate-anesthetized cats, using extracellular recording methods. Stimuli were 40-ms tone pulses presented through calibrated, sealed stimulating systems. In each animal, the CF (stimulus frequency to which the unit is most sensitive), threshold at CF, response/level function at CF, and binaural interactions were determined for isolated neurons (usually one per track) in 60–90 electrode tracks. For each unit, regardless of its CF, responses to 40 repetitions of contralateral tones of a single frequency, presented at each of four or five sound pressure levels (SPLs) in the range from 10 to 80 dB were obtained. Different test frequencies were used in each of four cats (1.6, 8.0, 11.0, and 16.0 kHz). For tones of each SPL, we generated maps of the response rates across the cortical surface. These maps were then superimposed on the more traditional maps of threshold CF. All units whose CF was equal to the test frequency could be driven at some SPL, given an appropriate monaural or binaural configuration of the stimulus. There was a clear spatial segregation of neurons according to the shapes of their CF tone response/level functions. Patches of cortex, often occupying more than 2 mm2, seemed to contain only monotonic or only nonmonotonic units. In three cortices, a patch of nonmonotonic cells was bounded ventrally by a patch of monotonie cells, and in one of these cases, a second patch of monotonic cells was found dorsal to the nonmonotonic patch. Contralateral tones of any given SPL evoked excitatory responses in discontinuous cortical territories. At low SPLs (10, 20 dB), small foci of activity occurred along the isofrequency line representing the test frequency. Many of these cells had nonmonotonic response/level functions. At mid- and high SPLs, the CFs of neurons activated by a pure tone varied across 3 octaves. At the highest SPL used (80 dB), most of the neurons with nonmonotonic response/level functions were inactive, or responded poorly; the active neurons were widely spread across the cortex, and the distribution of activity had a pattern bearing little relationship to the threshold CF contour map. These data indicate that only isolated patches of units within the relevant isofrequency contour are activated by a given suprathreshold contralateral tone. At suprathreshold stimulus levels, the region of cortex containing active patches extends widely beyond the threshold isofrequency contour region corresponding to the test stimulus frequency. The spatial representation of a stimulus delivered to the contralateral ear appears, therefore, to be highly level dependent and discontinuous. These observations suggest that in the cat's AI, tonotopicity and isofrequency contours are abstractions which bear little resemblance to the spatial representation of tonal signals.

On leave from: Departments of Psychology and Otolaryngology, Dalhousie University, Halifax, NS, Canada B3H 4J1
On leave from: Vision, Touch and Hearing Research Center, Department of Physiology and Pharmacology, The University of Queensland, Brisbane, Q1d, Australia 4072