A Rate Code for Sound Azimuth in Monkey Auditory Cortex: Implications for Human Neuroimaging Studies

Abstract

Is sound location represented in the auditory cortex of humans and monkeys? Human neuroimaging experiments have had only mixed success at demonstrating sound location sensitivity in primary auditory cortex. This is in apparent conflict with studies in monkeys and other animals, in which single-unit recording studies have found stronger evidence for spatial sensitivity. Does this apparent discrepancy reflect a difference between humans and animals, or does it reflect differences in the sensitivity of the methods used for assessing the representation of sound location? The sensitivity of imaging methods such as functional magnetic resonance imaging depends on the following two key aspects of the underlying neuronal population: (1) what kind of spatial sensitivity individual neurons exhibit and (2) whether neurons with similar response preferences are clustered within the brain.To address this question, we conducted a single-unit recording study in monkeys. We investigated the nature of spatial sensitivity in individual auditory cortical neurons to determine whether they have receptive fields (place code) or monotonic (rate code) sensitivity to sound azimuth. Second, we tested how strongly the population of neurons favors contralateral locations. We report here that the majority of neurons show predominantly monotonic azimuthal sensitivity, forming a rate code for sound azimuth, but that at the population level the degree of contralaterality is modest. This suggests that the weakness of the evidence for spatial sensitivity in human neuroimaging studies of auditory cortex may be attributable to limited lateralization at the population level, despite what may be considerable spatial sensitivity in individual neurons.

The neural code for interaural time difference in human auditory cortex

“…In hemifield tuning, neurons exhibit wide tuning curves with a flat maximum corresponding to sound sources either to the left or to the right. This type of tuning is consistent with the neural codes of auditory space found previously in single-unit studies of primate cortex 7 and MEG studies of the human brain 8 utilizing free-field stimuli. Therefore, it seems that in the human cortex the hemifield coding strategy applies to all horizontal sound source localization cues.…”

“…Neurophysiological evidence for this code has been found in small mammals 5,6 but it is unclear to what extent the results can be generalized to humans. Studies of spatial coding in the monkey 7 and human 8 auditory cortices have found receptive fields consistent with the hemifield code by utilizing free-field sound stimulation. It is, however, not clear what the contribution of ITD is in these results.…”

Modeling the categorical perception of speech sounds: A step toward biological plausibility

“…As a result, even small differences between sound stimuli led to large differences in the activity level, and this allowed for better discrimination-that is, perceptual expansionat the boundary. A similar association between discriminability and the shape of neuronal tuning curves has been demonstrated in the auditory cortex for the representation of sound source location (Stecker, Harrington, & Middlebrooks, 2005;Werner-Reiss & Groh, 2008). Localization is best for sound sources in frontal directions, although the majority of spatially sensitive neurons in the auditory cortex are maximally tuned to sound sources either to the left or to the right.…”

Neuronal representations of distance in human auditory cortex

“…There is also evidence from animal studies suggesting ILD neurons in primary auditory cortices, for example, in the cat (50) (note, however, that the link between animal physiology and human fMRI is relatively weak in the spatial auditory domain) (51). Further, our auditory systems are highly adaptive, and different cues may govern distance perception in different acoustic environments.…”