Monaural Spectral Contrast Mechanism for Neural Sensitivity to Sound Direction in the Medial Geniculate Body of the Cat

Abstract

Monaural spectral contrast mechanism for neural sensitivity to sound direction in the medial geniculate body of the cat. J. Neurophysiol. 78: 2754-2771, 1997. Central auditory neurons vary in sound direction sensitivity. Insensitive cells discharge well to all sound source directions, whereas sensitive cells discharge well to certain directions and poorly to others. High-frequency neurons in the latter group are differentially sensitive to binaural and monaural directional cues present in broadband noise (BBN). Binaural directional (BD) cells require binaural stimulation for directional sensitivity; monaural directional (MD) cells are sensitive to the direction of monaural stimuli. A model of MD sensitivity was tested using single-unit responses. The model assumes that MD cells derive directional sensitivity from pinna-derived spectral cues (head related transfer function, HRTF). This assumption was supported by the similarity of effects that pinna orientation produces on locations of HRTF patterns and on locations of MD cell azimuth function peaks and nulls. According to the model, MD neurons derive directional sensitivity by use of excitatory/inhibitory antagonism to compare sound pressure in excitatory and inhibitory frequency domains, and a variety of observations are consistent with this idea. 1) Frequency response areas of MD cells consist of excitatory and inhibitory domains. MD cells exhibited a higher proportion of multiple excitatory domains and narrower excitatory frequency domains than BD cells, features that may reflect specialization for spectral-dependent directional sensitivity. 2) MD sensitivity requires sound pressure in excitatory and inhibitory frequency domains. Directional sensitivity was evaluated using stimuli with frequency components confined exclusively to excitatory domains (E-only stimuli) or distributed in both excitatory and inhibitory domains (E/I stimuli). Each of 13 MD cells that were tested exhibited higher directional sensitivity to E/I than to E-only stimuli; most MD cells exhibited relatively low directional sensitivity when frequency components were confined exclusively to excitatory domains. 3) MD sensitivity derives from excitatory/inhibitory antagonism (spectral inhibition). Comparison of responses to best frequency and E/I stimuli provided strong support for spectral inhibition. Although spectral facilitation conceivably could contribute to directional sensitivity with direction-dependent increases in response, the results did not show this to be a significant factor. 4) Direction-dependent decreases in responsiveness to BBN reflect increased sound pressure in inhibitory relative to excitatory frequency domains. This idea was tested using the strength of two-tone inhibition, which is a function of stimulus levels in inhibitory relative to excitatory frequency domains. The finding that two-tone inhibition was stronger at directions where BBN responses were minimal than at directions where they were maximal supports the model.

Auditory Processing of Spectral Cues for Sound Localization in the Inferior Colliculus

“…DCN type IV units receive somatosensory inputs from the head and pinna and are similarly affected by pinna movements (Young et al 1995(Young et al , 1996. Our present characterization of type O units provides a solid foundation for investigating how the auditory processing of spectral information in the DCN and inferior colliculus contributes to spatial receptive fields in the thalamus (Imig et al 1997) and auditory cortex (Samson et al 1993). …”

“…Single-unit recordings in the medial geniculate body (MGB) of anesthetized cats suggest that type O outputs remain functionally segregated when they exit the inferior colliculus (Imig et al 1997). A thalamic expression of the DCN/ICC spectral processing pathway is implied by a subclass of neurons with closed excitatory tuning curves and monaural directional (MD) sensitivity.…”

Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

“…Such neurons are common throughout the mustached bat IC (Leroy and Wenstrup 2000;Mittmann and Wenstrup 1995;Nataraj and Wenstrup 2006;O'Neill 1985;Portfors and Wenstrup 1999) and occur in other species and auditory centers (Imig et al 1997;Kadia and Wang 2003;Portfors and Felix 2005;Rauschecker et al 1995;Sutter et al 1999).…”

Organization of Inhibitory Frequency Receptive Fields in Cat Primary Auditory Cortex

“…Although speculative, there is evidence that two-tone isRFs are related to the analysis of more complex signals. For example, two-tone inhibitory areas are necessary contributors to A1 cells' abilities to differentiate between frequency-modulated sweeps (e.g., Fuzessery and Hall 1996;Shamma et al 1993;Suga 1965), and monaural sound localization cues (Imig et al 1997). Two-tone isRFs can be used to predict cells' responses to spectrally complex sounds such as "ripple spectra" the energy of which is distributed across both esRF and isRF (Schreiner and Calhoun 1994;Shamma and Versnel 1995).…”

“…Typically, FTCs of auditory neurons have been defined with single-tone stimuli (analogous to single-spot light stimuli used to define the CRF) and have focused on the excitatory spectral RF (esRF). However, the effects of modulatory tones from outside of the esRF on responses to excitatory tones imply that single-tone tuning curves do not adequately characterize the spectral input of neurons (e.g., Imig et al 1997;Nelken et al 1994;Sachs and Kiang 1968;Suga and Tsuzuki 1985). As in the visual system, these influences should be crucial contributors to the analysis of complex sounds and auditory scenes.…”