1. We assessed mechanisms of binaural interaction underlying detection of interaural phase disparity (IPD) by recording single-unit responses in the superior olivary complex (SOC) of the anesthetized gerbil (Meriones unguiculatus). Binaural responses were obtained from 58 IPD-sensitive single units, 44 of which were histologically localized. Monaural responses were also obtained for 52 of 58 IPD-sensitive units. Additionally, responses were recorded from 16 units (best frequency < 2.4 kHz) in lateral SOC that were excited by ipsilateral stimulation and inhibited by contralateral stimulation (EI), none of which was IPD sensitive. Our results are consistent with a mechanism of binaural interaction 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 inhibitory inputs from the two ears. Despite the uniformity of binaural interactions, considerable diversity of temporal and monaural response properties was observed. 2. Monaural and binaural responses of 35 of 58 IPD-sensitive units were phase locked to the period of low-frequency (< 2.5 kHz) tones. Most phase-locking units were bilaterally excitable and, consistent with the coincidence-detection model, their IPD selectivity could be predicted from the difference between the mean phases of the monaural responses. The remaining units (23 of 58) did not phase lock in response to monaural or binaural tones. Most non-phase-locking units failed to respond to monaural stimulation of one or both ears (monaurally unresponsive units). 3. Some IPD-sensitive units were inhibited by monaural stimulation of the ipsilateral ear or both ears. A few units responded only at the onset of monaural and binaural tones. Phase locking was present in responses of some, but not all, of these monaurally 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 (MSO). IPD-sensitive units were also recorded in the lateral superior olive (LSO), in the superior paraolivary nucleus (SPN), and within a region forming a medial-dorsal cap around MSO. Bilaterally excitable unites were concentrated around MSO, but were also encountered in SPN, the medial-dorsal region, and LSO. Some monaurally unresponsive units were recorded in the vicinity of the MSO, but most were located in the medial-dorsal region. Monaurally inhibited units were localized to the medial border of the MSO cell column or to SPN. Onset units were localized to SPN and the medial-dorsal region. EI units were located exclusively in LSO.(ABSTRACT TRUNCATED AT 400 WORDS)
We used a combination of anatomical and physiological techniques to define the primary motor cortex (M1) of the marmoset monkey and its relationship to adjacent cortical fields. Area M1, defined as a region containing a representation of the entire body and showing the highest excitability to intracortical microstimulation, is architecturally heterogeneous: it encompasses both the caudal part of the densely myelinated "gigantopyramidal" cortex (field 4) and a lateral region, corresponding to the face representation, which is less myelinated and has smaller layer 5 pyramidal cells (field 4c). Rostral to M1 is a field that is strongly reminiscent of field 4 in terms of cyto- and myeloarchitecture but that in the marmoset is poorly responsive to microstimulation. Anatomical tracing experiments revealed that this rostral field is interconnected with visual areas of the posterior parietal cortex, whereas M1 itself has no such connections. For these reasons, we considered this field to be best described as part of the dorsal premotor cortex and adopted the designation 6Dc. Histological criteria were used to define other fields adjacent to M1, including medial and ventral subdivisions of the premotor cortex (fields 6M and 6V) and the rostral somatosensory field (area 3a), as well as a rostral subdivision of the dorsal premotor area (field 6Dr). These results suggest a basic plan underlying the histological organization of the caudal frontal cortex in different simian species, which has been elaborated during the evolution of larger species of primate by creation of further morphological and functional subdivisions.
1. Motion of sound sources results in temporal variation of the binaural cues for sound localization. We evaluated the influence of virtual motion on neural tuning to one of these cues, interaural phase disparity (IPD). Responses to dichotic stimuli were recorded from single units in the inferior colliculus of the anesthetized cat and gerbil (Meriones unguiculatus). Static IPDs were generated by presenting dichotic tone pairs with a constant phase offset maintained for the duration of the stimulus. Time-varying IPDs were generated by simultaneously presenting a pure tone to one ear and a phase-modulated tone to the other ear. Sets of time-varying stimuli consisted of modulations through partially overlapping ranges of IPD, corresponding to movement of a sound source through partially overlapping arcs in the horizontal plane. 2. In agreement with previous results, neuronal discharge was typically a peaked function of static IPD resulting from both binaural facilitation at favorable IPDs and binaural suppression at unfavorable IPDs. Responses to time-varying IPD stimuli appeared to be shaped by the same facilitative and inhibitory mechanisms that underlie static IPD tuning. Modulation toward the peak of binaural facilitation increased the probability of discharge, and modulation toward the peak of binaural suppression decreased the probability of discharge. However, it was also clear that IPD tuning could be significantly altered by the temporal context of the stimulus. For the vast majority of units in response to modulation through partially overlapping ranges of IPD the discharge rate profiles were generally nonoverlapping. This shift in IPD tuning induced by the virtual motion reflects the fact that the binaural interaction associated with a given IPD depends on the recent history of stimulation. In addition, modulation in opposite directions through the same range of IPDs often elicited asymmetric responses. These nonlinearities imply that most inferior colliculus neurons do not unambiguously encode a specific IPD, but instead may encode small changes of IPD occurring virtually anywhere within their receptive fields. In a few cases modulation through overlapping ranges of IPD elicited contiguous response profiles, indicating that for these units responses were determined entirely by instantaneous IPD. 3. The nonlinearity of responses to time-varying IPD stimuli could not be attributed to monaural entrainment to the phase-modulated signals, did not depend on the phase modulation waveform, and occurred irrespective of which ear received the phase-modulated signal. Responses were similar in cats and gerbils, suggesting that the underlying mechanisms are common to binaural processing in diverse mammalian species.(ABSTRACT TRUNCATED AT 400 WORDS)
The owl can discriminate changes in the location of sound sources as small as 3 degrees and can aim its head to within 2 degrees of a source. A typical neuron in its midbrain space map has a spatial receptive field that spans 40 degrees--a width that is many times the behavioural threshold. Here we have quantitatively examined the relationship between neuronal activity and perceptual acuity in the auditory space map in the barn owl midbrain. By analysing changes in firing rate resulting from small changes of stimulus azimuth, we show that most neurons can reliably signal changes in source location that are smaller than the behavioural threshold. Each source is represented in the space map by a focus of activity in a population of neurons. Displacement of the source causes the pattern of activity in this population to change. We show that this change predicts the owl's ability to detect a change in source location.
Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity. J. Neurophysiol. 80: 3062-3076, 1998. Previous studies demonstrated that tuning of inferior colliculus (IC) neurons to interaural phase disparity (IPD) is often profoundly influenced by temporal variation of IPD, which simulates the binaural cue produced by a moving sound source. To determine whether sensitivity to simulated motion arises in IC or at an earlier stage of binaural processing we compared responses in IC with those of two major IPD-sensitive neuronal classes in the superior olivary complex (SOC), neurons whose discharges were phase locked (PL) to tonal stimuli and those that were nonphase locked (NPL). Time-varying IPD stimuli consisted of binaural beats, generated by presenting tones of slightly different frequencies to the two ears, and interaural phase modulation (IPM), generated by presenting a pure tone to one ear and a phase modulated tone to the other. IC neurons and NPL-SOC neurons were more sharply tuned to time-varying than to static IPD, whereas PL-SOC neurons were essentially uninfluenced by the mode of stimulus presentation. Preferred IPD was generally similar in responses to static and time-varying IPD for all unit populations. A few IC neurons were highly influenced by the direction and rate of simulated motion, but the major effect for most IC neurons and all SOC neurons was a linear shift of preferred IPD at high rates-attributable to response latency. Most IC and NPL-SOC neurons were strongly influenced by IPM stimuli simulating motion through restricted ranges of azimuth; simulated motion through partially overlapping azimuthal ranges elicited discharge profiles that were highly discontiguous, indicating that the response associated with a particular IPD is dependent on preceding portions of the stimulus. In contrast, PL-SOC responses tracked instantaneous IPD throughout the trajectory of simulated motion, resulting in highly contiguous discharge profiles for overlapping stimuli. This finding indicates that responses of PL-SOC units to time-varying IPD reflect only instantaneous IPD with no additional influence of dynamic stimulus attributes. Thus the neuronal representation of auditory spatial information undergoes a major transformation as interaural delay is initially processed in the SOC and subsequently reprocessed in IC. The finding that motion sensitivity in IC emerges from motion-insensitive input suggests that information about change of position is crucial to spatial processing at higher levels of the auditory system.
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