NEURONS SENSITIVE TO INTERAURAL PHASE DISPARITY IN GERBIL SUPERIOR OLIVE - DIVERSE MONAURAL AND TEMPORAL RESPONSE PROPERTIES

1. We assessed mechanisms of binaural interaction underlying detection of interaural phase disparity (IPD) by recording single-unit response s in the superior olivary complex (SOC) of the anesthetized gerbil (Me riones unguiculatus). Binaural responses were obtained from 58 IPD-sen sitive single units, 44 of which were histologically localized. Monaur al responses were also obtained for 52 of 58 IPD-sensitive units. Addi tionally, responses were recorded from 16 units (best frequency < 2.4 kHz) in lateral SOC that were excited by ipsilateral stimulation and i nhibited by contralateral stimulation (EI), none of which was IPD sens itive. Our results are consistent with a mechanism of binaural interac tion involving detection of coincident excitatory inputs from the two ears. There was no compelling evidence of-binaural sensitivity arising from IPD-dependent interactions of phase-locked excitatory and inhibi tory inputs from the two ears. Despite the uniformity of binaural inte ractions, considerable diversity of temporal and monaural response pro perties was observed. 2. Monaural and binaural responses of 35 of 58 I PD-sensitive units were phase locked to the period of low-frequency (< 2.5 kHz) tones. Most phase-locking units were bilaterally excitable an d, consistent with the coincidence-detection model, their IPD selectiv ity could be predicted from the difference between the mean phases of the monaural responses. The remaining units (23 of 58) did not phase l ock in response to monaural or binaural tones. Most non-phase-locking units failed to respond to monaural stimulation of one or both ears (m onaurally unresponsive units). 3. Some IPD-sensitive units were inhibi ted by monaural stimulation of the ipsilateral ear or both ears. A few units responded only at the onset of monaural and binaural tones. Pha se locking was present in responses of some, but not all, of these mon aurally inhibited and onset units. 4. Most IPD-sensitive neurons were encountered at sites within or immediately adjacent to the cell column of the medial superior olive (MSG). IPD-sensitive units were also rec orded in the lateral superior olive (LSO), in the superior paraolivary nucleus (SPN), and within a region forming a medial-dorsal cap around MSG. Bilaterally excitable units were concentrated around MSG, but we re also encountered in SPN, the medial-dorsal region, and LSO. Some mo naurally unresponsive units were recorded in the vicinity of MSG, but most were located in the medial-dorsal region. Monaurally inhibited un its were localized to the medial border of the MSO cell column or to S PN. Onset units were localized to SPN and the medial-dorsal region. EI units were located exclusively in LSO. 5. Despite the diversity of mo naural and temporal response properties, binaural interactions underly ing IPD tuning were remarkably uniform. Responses were generated at be st IPD by facilitation or summation (45 of 46 units) and at worst IPD by suppression or occlusion (35 of 41 units). No differences were evid ent in the binaural interactions underlying IPD tuning of units with d iffer ent monaural and temporal response properties or locations. 6. I PD tuning was characterized at multiple tone frequencies for 34 units. For most units, the interaural time difference (ITD) tuning functions computed at multiple frequencies coincided at their peaks. There were no significant differences between means for units with different mon aural and temporal response properties. Most units (81%) had character istic delays corresponding to delays of the stimulus at the ipsilatera l ear (mean 241 mu s). 7. Mean binaural response latencies for phase-l ocking and nonphase-locking units were 5.1 +/- 0.2 (SE) ms and 12.5 +/ - 1.6 ms, respectively. Mean latencies of non-phase-locking units were significantly different from those of phase-locking units (P < 0.05), but were not significantly different from those of inferior colliculu s neurons. 8. These data are consistent with a neural mechanism of IPD coding involving detection of coincidence of excitatory events origin ating from the two ears. Synaptic inhibition within MSO may participat e in IPD coding by modulating this excitatory-excitatory interaction. The diversity of monaural and temporal response properties may be indi cative of functionally and anatomically distinct populations of IPD-se nsitive neurons within the gerbil SOC. It is proposed that phase-locki ng units correspond to primary binaural comparators and that non-phase -locking units correspond to higher-order binaural neurons.