Recanzone, Gregg H., Darren C. Guard, and Mimi L. Phan. Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey. J. Neurophysiol. 83: 2315Neurophysiol. 83: -2331Neurophysiol. 83: , 2000. Response properties of auditory cortical neurons measured in anesthetized preparations have provided important information on the physiological differences between neurons in different auditory cortical areas. Studies in the awake animal, however, have been much less common, and the physiological differences noted may reflect differences in the influence of anesthetics on neurons in different cortical areas. Because the behaving monkey is gaining popularity as an animal model in studies exploring auditory cortical function, it has become critical to physiologically define the response properties of auditory cortical neurons in this preparation. This study documents the response properties of single cortical neurons in the primary and surrounding auditory cortical fields in monkeys performing an auditory discrimination task. We found that neurons with the shortest latencies were located in the primary auditory cortex (AI). Neurons in the rostral field had the longest latencies and the narrowest intensity and frequency tuning, neurons in the caudomedial field had the broadest frequency tuning, and neurons in the lateral field had the most monotonic rate/level functions of the four cortical areas studied. These trends were revealed by comparing response properties across the population of studied neurons, but there was considerable variability between neurons for each response parameter other than characteristic frequency (CF) in each cortical area. Although the neuronal CFs showed a systematic spatial organization across AI, no such systematic organization was apparent for any other response property in AI or the adjacent cortical areas. The results of this study indicate that there are physiological differences between auditory cortical fields in the behaving monkey consistent with previous studies in the anesthetized animal and provide insights into the functional role of these cortical areas in processing acoustic information. I N T R O D U C T I O NStudies in the macaque monkey auditory cortex have defined several cortical fields based on physiological, anatomic, and combined techniques

In both humans and songbirds, infants learn vocalizations by imitating the sounds of adult tutors with whom they interact during an early sensitive period. Vocal learning occurs in few animal taxa; similarities in the imitation process between humans and songbirds make the songbird a unique system in which vocal learning mechanisms can be studied at the neurobiological level. One theory of vocal learning proposes that early auditory experience generates auditory memories that subsequently guide vocal imitation. We now present a combination of behavioral and neurophysiological results, obtained in a songbird, that support this theory. We show that neurons in a forebrain auditory area of adult male zebra finches are selectively tuned to the song of a tutor heard early in development. Furthermore, the strength of this selectivity shows a striking correlation with the fidelity of vocal imitation, suggesting that this auditory memory may have served as the model for song learning.development ͉ electrophysiology ͉ memory ͉ caudal medial nidopallium ͉ zebra finch

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 approximately 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 degrees 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.

The role of GABA in the central processing of complex auditory signals is not fully understood. We have studied the involvement of GABA A-mediated inhibition in the processing of birdsong, a learned vocal communication signal requiring intact hearing for its development and maintenance. We focused on caudomedial nidopallium (NCM), an area analogous to parts of the mammalian auditory cortex with selective responses to birdsong. We present evidence that GABA A-mediated inhibition plays a pronounced role in NCM's auditory processing of birdsong. Using immunocytochemistry, we show that approximately half of NCM's neurons are GABAergic. Whole cell patch-clamp recordings in a slice preparation demonstrate that, at rest, spontaneously active GABAergic synapses inhibit excitatory inputs onto NCM neurons via GABA A receptors. Multi-electrode electrophysiological recordings in awake birds show that local blockade of GABA A-mediated inhibition in NCM markedly affects the temporal pattern of song-evoked responses in NCM without modifications in frequency tuning. Surprisingly, this blockade increases the phasic and largely suppresses the tonic response component, reflecting dynamic relationships of inhibitory networks that could include disinhibition. Thus processing of learned natural communication sounds in songbirds, and possibly other vocal learners, may depend on complex interactions of inhibitory networks.