Modulation of Level Response Areas and Stimulus Selectivity of Neurons in Cat Primary Auditory Cortex

Abstract

Zhang, Jiping, Kyle T. Nakamoto, and Leonard M. Kitzes. Modulation of level response areas and stimulus selectivity of neurons in cat primary auditory cortex. J Neurophysiol 94: 2263-2274, 2005. First published May 25, 2005 10.1152/jn.01207.2004. Sounds commonly occur in sequences, such as in speech. It is therefore important to understand how the occurrence of one sound affects the response to a subsequent sound. We approached this question by determining how a conditioning stimulus alters the response areas of single neurons in the primary auditory cortex (AI) of barbiturate-anesthetized cats. The response areas consisted of responses to stimuli that varied in level at the two ears and delivered at the characteristic frequency of each cell. A binaural conditioning stimulus was then presented Ն50 ms before each of the stimuli comprising the level response area. An effective preceding stimulus alters the shape and severely reduces the size and response magnitude of the level response area. This ability of the preceding stimulus depends on its proximity in the level domain to the level response area, not on its absolute level or on the size of the response it evokes. Preceding stimuli evoke a nonlinear inhibition across the level response area that results in an increased selectivity of a cortical neuron for its preferred binaural stimuli. The selectivity of AI neurons during the processing of a stream of acoustic stimuli is likely to be restricted to a portion of their level response areas apparent in the tone-alone condition. Thus rather than being static, level response areas are fluid; they can vary greatly in extent, shape and response magnitude. The dynamic modulation of the level response area and level selectivity of AI neurons might be related to several tasks confronting the central auditory system. I N T R O D U C T I O NAs acoustic stimuli commonly occur in a temporal relation to other acoustic stimuli, it is important to understand how responses of cortical neurons vary during the processing of a stream of acoustic signals. Throughout the auditory neuroaxis, discharge rate as a function of monaural stimulus level (so called rate-level functions) have been shown to be displaced to higher stimulus levels when stimuli are presented either during or after a conditioning stimulus (Boettcher et

Level Dependence of Contextual Modulation in Auditory Cortex

“…We found, as have others, that suppression was stronger for maskers that were higher level and closer to characteristic frequency (Bartlett and Wang 2005;Brosch and Schreiner 1997;Calford and Semple 1995;Malone and Semple 2001;Shamma and Symmes 1985). Similarly for other stimulus parameters such as binaural levels or spatial location, maskers cause stronger suppression the closer they are to a neuron's preferred stimulus (Reale and Brugge 2000;Zhang et al 2005). We found that increasing the intensity of the probe reduced the amount of suppression, consistent with a straightforward competitive interaction between the probe response and the suppression induced by the masker.…”

“…We conclude that forward suppression probably includes contributions from both response-gain control and level-gain control. In contrast, forward suppression of responses to different binaural level combinations appears to act by response-gain control and not level-gain control (Nakamoto et al 2006;Zhang et al 2005). Although our free-field stimulus reached both ears, we did not independently vary binaural levels and thus do not know whether the binaural response properties of our neurons showed response-gain control, level-gain control, or both.…”

“…Stimuli presented outside the classical receptive field can modulate the response to stimuli at the center of the receptive field in visual, somatosensory, and auditory cortical neurons (Allman et al 1985;Brosch and Schreiner 1997;Calford and Semple 1995;Nelson and Frost 1978;Phillips and Cynader 1985;Reale and Brugge 2000;Simons 1985;Zhang et al 2005). These contextual interactions include both suppression and facilitation and may be involved in perceptual grouping effects such as figure-ground segmentation, contour completion, forward masking, and other aspects of visual or auditory scene analysis (Albright and Stoner 2002;Micheyl et al 2007).…”

Temporal Nonlinearity During Recovery From Sequential Inhibition by Neurons in the Cat Primary Auditory Cortex

“…The occurrence of a preceding stimulus can reduce the entire level response area (Reale and Brugge 2000;Zhang et al 2005). The magnitude of such sequential inhibition varies systematically in a nonlinear manner across the level response area.…”

“…(We use the phrase "sequential inhibition" to refer to the impact of a preceding stimulus on the response to a succeeding stimulus and the term "inhibition" to refer to the reduction of a response with no implication of a mechanism causing the reduction.) For a given preceding stimulus, the inhibition of responses to stimuli within the PBC is least; the inhibition increases progressively for stimuli that are progressively more remote from the PBC (Zhang et al 2005). The ability of a preceding binaural stimulus to inhibit the response to a succeeding binaural stimulus depends on its proximity to the PBC rather than on its absolute binaural levels (Zhang et al 2005).…”