Despite four decades of research, the nature of the neural representation of sound location in the auditory cortex remains unclear. Previous studies have failed to identify any maps or patches of spatial representation in the mammalian auditory cortex (Middlebrooks and Pettigrew, 1981, J Neurosci; Middlebrooks, 2021, J Neurosci). A prevailing hypothesis of cortical spatial processing is the distributed population coding, supported by the evidence that neurons respond broadly to sound locations on the contralateral hemifield (Ortiz-Rios et al., 2017, Neuron; van der Heijden et al., 2019, Nat Rev Neurosci). However, electrophysiology and fMRI methods have limited spatial resolution to evaluate the cortical representation of sound locations.
In the present study, we took advantage of the flat brain of the marmoset, a highly vocal New World monkey, and used wide-field calcium imaging methods to investigate the neural representations of sound location in the auditory cortex and neighboring multisensory regions (fundus of superior temporal, FST; medial superior temporal, MST) in awake condition.
Most cortical areas preferred contralateral sound locations, but regions tuned to the front and ipsilateral locations formed five to ten patches. We found those patches in both primary and nonprimary, rostral and caudal auditory cortex.
Next, we investigated whether spatial tuning of patches depends on interaural time and level differences (ITD and ILD) cues. We found patches that prefer low frequency were ITD cue dependent. In contrast, patches that prefer high frequency were cue independent. Patches identified with spatial and binaural stimuli were relatively stable across sound levels.
Furthermore, a neighboring multisensory FST/MST has weak sound-driven responses and was not topographically organized by sound frequency. Surprisingly, FST/MST was organized topographically by sound locations that range from far-contralateral to front.
Finally, a horizontal visual stimulus will evoke a strong response only in the FST/MST but not in the auditory cortex. We also identified a retinotopic map in the FST/MST. Notably, multisensory auditory and visual-spatial maps in the FST/MST largely overlapped.
In summary, our data suggest that auditory space is represented in the cortex by patch and map.