The Journal of Neurophysiology Vol. 83 No. 5 May 2000, pp. 2723-2739
Copyright ©2000 by the American Physiological Society

Correlation Between the Activity of Single Auditory Cortical Neurons and Sound-Localization Behavior in the Macaque Monkey

 ¹Center for Neuroscience and  ²Section of Neurobiology, Physiology and Behavior, University of California, Davis, California 95616

Recanzone, Gregg H., Darren C. Guard, Mimi L. Phan, and Tien-I K. Su. Correlation Between the Activity of Single Auditory Cortical Neurons and Sound-Localization Behavior in the Macaque Monkey. J. Neurophysiol. 83: 2723-2739, 2000. Lesion studies have indicated that the auditory cortex is crucial for the perception of acoustic space, yet it remains unclear how these neurons participate in this perception. To investigate this, we studied the responses of single neurons in the primary auditory cortex (AI) and the caudomedial field (CM) of two monkeys while they performed a sound-localization task. Regression analysis indicated that the responses of ~80% of neurons in both cortical areas were significantly correlated with the azimuth or elevation of the stimulus, or both, which we term "spatially sensitive." The proportion of spatially sensitive neurons was greater for stimulus azimuth compared with stimulus elevation, and elevation sensitivity was primarily restricted to neurons that were tested using stimuli that the monkeys also could localize in elevation. Most neurons responded best to contralateral speaker locations, but we also encountered neurons that responded best to ipsilateral locations and neurons that had their greatest responses restricted to a circumscribed region within the central 60° of frontal space. Comparing the spatially sensitive neurons with those that were not spatially sensitive indicated that these two populations could not be distinguished based on either the firing rate, the rate/level functions, or on their topographic location within AI. Direct comparisons between the responses of individual neurons and the behaviorally measured sound-localization ability indicated that proportionally more neurons in CM had spatial sensitivity that was consistent with the behavioral performance compared with AI neurons. Pooling the responses across neurons strengthened the relationship between the neuronal and psychophysical data and indicated that the responses pooled across relatively few CM neurons contain enough information to account for sound-localization ability. These data support the hypothesis that auditory space is processed in a serial manner from AI to CM in the primate cerebral cortex.

Colloquium Paper
Spatial processing in the auditory cortex of the macaque monkey

Center for Neuroscience and Section of Neurobiology, Physiology, and Behavior, University of California, 1544 Newton Court, Davis, CA 95616

The patterns of cortico-cortical and cortico-thalamic connections of auditory cortical areas in the rhesus monkey have led to the hypothesis that acoustic information is processed in series and in parallel in the primate auditory cortex. Recent physiological experiments in the behaving monkey indicate that the response properties of neurons in different cortical areas are both functionally distinct from each other, which is indicative of parallel processing, and functionally similar to each other, which is indicative of serial processing. Thus, auditory cortical processing may be similar to the serial and parallel "what" and "where" processing by the primate visual cortex. If "where" information is serially processed in the primate auditory cortex, neurons in cortical areas along this pathway should have progressively better spatial tuning properties. This prediction is supported by recent experiments that have shown that neurons in the caudomedial field have better spatial tuning properties than neurons in the primary auditory cortex. Neurons in the caudomedial field are also better than primary auditory cortex neurons at predicting the sound localization ability across different stimulus frequencies and bandwidths in both azimuth and elevation. These data support the hypothesis that the primate auditory cortex processes acoustic information in a serial and parallel manner and suggest that this may be a general cortical mechanism for sensory perception.