Organization of Inhibitory Frequency Receptive Fields in Cat Primary Auditory Cortex

Abstract

. Organization of inhibitory frequency receptive fields in cat primary auditory cortex. J. Neurophysiol. 82: 2358Neurophysiol. 82: -2371Neurophysiol. 82: , 1999. Based on properties of excitatory frequency (spectral) receptive fields (esRFs), previous studies have indicated that cat primary auditory cortex (A1) is composed of functionally distinct dorsal and ventral subdivisions. Dorsal A1 (A1d) has been suggested to be involved in analyzing complex spectral patterns, whereas ventral A1 (A1v) appears better suited for analyzing narrowband sounds. However, these studies were based on single-tone stimuli and did not consider how neuronal responses to tones are modulated when the tones are part of a more complex acoustic environment. In the visual and peripheral auditory systems, stimulus components outside of the esRF can exert strong modulatory effects on responses. We investigated the organization of inhibitory frequency regions outside of the pure-tone esRF in single neurons in cat A1. We found a high incidence of inhibitory response areas (in 95% of sampled neurons) and a wide variety in the structure of inhibitory bands ranging from a single band to more than four distinct inhibitory regions. Unlike the auditory nerve where most fibers possess two surrounding "lateral" suppression bands, only 38% of A1 cells had this simple structure. The word lateral is defined in this sense to be inhibition or suppression that extends beyond the low-and high-frequency borders of the esRF. Regional differences in the distribution of inhibitory RF structure across A1 were evident. In A1d, only 16% of the cells had simple two-banded lateral RF organization, whereas 50% of A1v cells had this organization. This nonhomogeneous topographic distribution of inhibitory properties is consistent with the hypothesis that A1 is composed of at least two functionally distinct subdivisions that may be part of different auditory cortical processing streams.

Level Dependence of Contextual Modulation in Auditory Cortex

“…In this neuron, a 2-kHz masker had little effect on the response to the 6-kHz probe, whereas a 7-kHz masker completely suppressed the response to the same probe. Thus strong masking was evoked by tones near the characteristic frequency (6 kHz for this cell) as was typical for the cells in our sample and consistent with previous reports (Brosch and Schreiner 1997;Calford and Semple 1995;Sutter et al 1999;Tai and Zador 2001).…”

“…We quantified tone-evoked hyperpolarization by measuring minimum membrane potential for isolated tone responses, relative to rest, in a fixed window 0 -350 ms after tone onset. We quantified suppressive bandwidth as the contiguous region in which spiking responses were reduced below a criterion of spontaneous spike count ϩ20% of peak spike count (Sutter and Schreiner 1991;Sutter et al 1999).…”

“…This raises the question of whether auditory cortical neurons, like visual and somatosensory cortical neurons, exhibit a similar cross-over between facilitation and suppression depending on the relative level of the probe. In primary auditory cortex, however, contextual interactions have generally been studied at only a single probe level Schreiner 2000, 1997;Calford and Semple 1995;Malone and Semple 2001;Shamma and Symmes 1985;Sutter et al 1999). It is therefore unknown whether the relative intensity of masker and probe stimuli regulates whether contextual interactions in auditory cortical neurons are facilitative or suppressive.…”

Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex

“…NB and BB neurons within the same isofrequency contour should be interconnected if they responded linearly to spectral information alone, because their spectral sensitivities would overlap completely; however, this is not the case. Exclusive connections between similar bandwidth compartments may arise because NB and BB neurons have other contrasting spectrotemporal properties, including the pattern of surround inhibition, intensity dependence, sensitivity to broadband stimuli, and FM sweep selectivities (15,16,27,31,32). Thus, NB and BB neurons form spatially and functionally distinct modules, and AI intrinsic connections support this segregation.…”

Development of spectral and temporal response selectivity in the auditory cortex

“…1b; see Fig. 7, which is published as supporting information on the PNAS web site, for schematic of stimulus presentations) (13)(14)(15). The probe tone frequency that was used in these studies was the ERF characteristic frequency (CF), delivered 10-15 dB above response threshold.…”