Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex

Abstract

1. The physiology and topography of single neuron responses along the isofrequency domain of the middle- and high-frequency portions [characteristic frequencies (CFs) greater than 4 kHz] of the primary auditory cortex (AI) were investigated in the barbiturate-anesthetized cat. Single neurons were recorded at several locations along the extent of isofrequency contours, defined from initial multiple-unit mapping. For each neuron a high-resolution excitatory tuning curve was determined, and for some neurons high-resolution two-tone tuning curves were recorded to measure inhibitory/suppressive areas. 2. A physiologically distinct population of neurons was found in the dorsal part of cat AI. These neurons exhibited two or three distinct excitatory frequency ranges, whereas most neurons in AI responded with excitation to a single narrow frequency range. These were called multipeaked neurons because of the shape of their tuning curves. At frequencies between the excitatory regions, the multipeaked neurons were inhibited or unresponsive. 3. Multipeaked neurons exhibited several distinct threshold minima in their frequency tuning curves. Most of the multipeaked neurons (88%) displayed two frequency minima, whereas the rest exhibited three minima. 4. The frequency separation between threshold minima was less than 1 octave in 71% of the double-peaked neurons recorded. Occasionally, the frequency peaks of these neurons closely corresponded to a response to second and third harmonics without a response to the fundamental frequency. 5. Multipeaked neurons exhibited a wide range of total bandwidths (highest excitatory frequency minus lowest excitatory frequency expressed in octaves). Bandwidths of the isolated peaks within the same neuron were also quite variable. 6. Response latencies to tones with frequencies within each peak of a multipeaked neuron could vary considerably. In 71% (17) of the neurons, tones corresponding to the high-frequency peak (CFh) elicited a longer response latency (greater than 4 ms) than those corresponding to the low-frequency peak (CF1). 7. Inhibitory/suppressive bands, as demonstrated with a two-tone paradigm, were often present between the peaks. Typically, neurons with excitatory peaks of similar response latencies showed an inhibitory band located between the peaks. 8. Ninety percent of the topographically localized multipeaked neurons were in the dorsal part of AI (greater than 1 mm dorsal to the maximum in the sharpness-of-tuning map). Although these neurons were restricted to dorsal AI, only 35% of neurons in this region were multipeaked. 9. Multipeaked neurons could show decreased response latencies and thresholds to two-tone combinations.(ABSTRACT TRUNCATED AT 400 WORDS)

Reorganization of receptive fields following hearing loss in inferior colliculus neurons

“…The neural response to each frequency/ intensity combination is represented by a vertical line, with the thickness of each line proportional to the number of spikes. Following the method of Sutter and Schreiner (1991), the spontaneous count was estimated by averaging the spike counts in the 9-frequency by 5-intensity array located at the lower left (low intensity, low frequency) corner of the FRA, outside the range of response. The data were then smoothed using a 3-frequency by 3-intensity moving average, and the smoothed spike counts were compared to the estimated spontaneous count.…”

“…Each tone was presented once in pseudorandom order, but for units with low response rates up to 2 additional samples were taken. This procedure is adapted from Sutter and Schreiner (1991).…”

Spatial sensitivity of neurons in the anterior, posterior, and primary fields of cat auditory cortex

“…Here, frequency tuning was assessed using 80-ms pure tones having frequencies ranging from 0.5 to 30 kHz in 1/6-octave steps, and levels ranging from −10 to 50 or 60 dB SPL in 10-dB steps. The CF was defined as the frequency of the tuning peak exhibiting the lowest threshold, where threshold was defined as a spike count equal to 40% of the unit's maximum (Stecker et al 2005a;Sutter and Schreiner 1991). In this report, the CF is said to be undefined if the FRA lacked coherent structure; a few units were excluded from the CF sample because they were not tested at a sufficiently low SPL.…”

“…There is also evidence that multi-peaked frequency response areas (FRAs) may be more common in PAF and AAF than in ventral A1 (Knight 1977;Loftus and Sutter 2001). Although Sutter and Schreiner (1991) described a number of neurons with multi-peaked FRAs in A1, > 90% of these were located in the field's dorsal region near the suprasylvian sulcus. That region probably corresponded to the "dorsal zone" (DZ; Middlebrooks and Zook 1983), an area that we now regard as a distinct auditory field (Stecker et al 2005a).…”

Excitatory, inhibitory and facilitatory frequency response areas in the inferior colliculus of hearing impaired mice

“…Spectral integration by single neurons is evidenced by neurons with multiple frequency tuning peaks, enhanced sensitivity to noise, or combination sensitivity; facilitated or enhanced responses to the combination of two distinctly different frequency elements (Brosch et al, 1999;Fuzessery and Feng, 1983;Kadia and Wang, 2003;Ohl and Scheich, 1997;Rauschecker, 1998;Rauschecker et al, 1995;Schreiner and Cynader, 1984;Suga and O'Neill, 1979;Sutter and Schreiner, 1991). Recent evidence suggests that neurons that integrate across frequencies first occur in the inferior colliculus (IC) (Marsh et al, 2006;Portfors and Wenstrup, 2001b;Wenstrup and Leroy, 2001).…”