Broadband onset inhibition can suppress spectral splatter in the auditory brainstem.

In vivo intracellular responses to auditory stimuli revealed that, in a particular population of cells of the ventral nucleus of the lateral lemniscus (VNLL) of rats, fast inhibition occurred before the first action potential. These experimental data were used to constrain a leaky integrate-and-fire (LIF) model of the neurons in this circuit. The post-synaptic potentials of the VNLL cell population were characterized using a method of triggered averaging. Analysis suggested that these inhibited VNLL cells produce action potentials in response to a particular magnitude of the rate of change of their membrane potential. The LIF model was modified to incorporate the VNLL cells' distinctive action potential production mechanism. The model was used to explore the response of the population of VNLL cells to simple speech-like sounds. These sounds consisted of a simple tone modulated by a saw tooth with exponential decays, similar to glottal pulses that are the repeated impulses seen in vocalizations. It was found that the harmonic component of the sound was enhanced in the VNLL cell population when compared to a population of auditory nerve fibers. This was because the broadband onset noise, also termed spectral splatter, was suppressed by the fast onset inhibition. This mechanism has the potential to greatly improve the clarity of the representation of the harmonic content of certain kinds of natural sounds.

Intracellular responses and morphology of rat ventral complex of the lateral lemniscus neurons in vivo.

The function of the ventral and intermediate nuclei of the lateral lemniscus (VNLL and INLL), collectively termed ventral complex of the lateral lemniscus (VCLL), is unclear. Several studies have suggested that it plays a role in coding the temporal aspects of sound. In our study, a sample (n = 161) of intracellular responses to dichotically presented noise or tone bursts was collected from the VCLL of urethane-anesthetized rats in vivo. Intracellular recordings revealed six distinct response types to tones, distinguished by their synaptic and membrane characteristics as well as firing pattern. Three of these response types were correlated with distinct cellular morphologies revealed by intracellular injection of neurobiotin. 3D reconstructions of recorded neurons within the VCLL showed the spatial distribution of various response properties, including response type, laterality, characteristic frequency (CF), and binaural influences. Cells that responded to monaural (55%) or binaural (45%) stimulation were distributed throughout the VCLL. Almost all VCLL units were responsive to contralateral stimulation (97%). Most neurons were excited by contralateral stimulation (83%), many exclusively (43%), and some in conjunction with ipsilateral inhibition (28%) or excitation (12%). The INLL contained mostly binaural neurons (65%), typically with ipsilateral inhibition and contralateral excitation. These results indicate that the VCLL is not a monaural structure and there is a dorsal-ventral segregation of binaural and monaural cells. 3D reconstructions of intracellular CFs did not reveal the presence of any tonotopic arrangement within the VCLL. Presumably, the proposed timing role of this structure does not require a systematic representation of tonal frequency.

Powerful, onset inhibition in the ventral nucleus of the lateral lemniscus.

The function of the ventral nucleus of the lateral lemniscus (VNLL), a secondary processing site within the auditory brain stem, is unclear. It is known to be a major source of inhibition to the inferior colliculus (IC). It is also thought to play a role in coding the temporal aspects of sound, such as onsets and the periodic components of complex stimuli. In vivo intracellular recordings from VNLL neurons (n = 56) in urethane anesthetized rats revealed the presence of large-amplitude, short-duration, onset inhibition in a subset of neurons (14.3%). This inhibition occurred before the first action potential (AP) elicited by noise or tone bursts, was broadly tuned to tonal frequency and was shown to delay the first AP. Our data suggest it is a result of an intrinsic circuit activated by the octopus cell pathway originating in the contralateral cochlear nucleus; this pathway is known to convey exquisitely timed and broadly tuned onset information. This powerful inhibition within the VNLL appears to control the timing of this structure's inhibitory output to higher centers, which has important auditory processing outcomes. The circuit also provides a pathway for fast, broadly tuned, onset inhibition to the IC.

Balanced inhibition and excitation underlies spike firing regularity in ventral cochlear nucleus chopper neurons.

Ventral cochlear nucleus stellate cells respond to characteristic frequency (CF) tones with sustained (C(S)), transient (C(T)) or onset chopping (O(C)) activity. The mechanisms underlying these different response patterns are not fully understood, and the present study used in vivo intracellular recordings (n = 42) in urethane-anaesthetized rats to examine the possible influence of inhibition on action potential regularity. Hyperpolarization following the offset of a CF tone burst was used as a measure of on-CF inhibition. A cluster analysis based on several membrane potential features, including on-CF inhibition, discriminated three groups in addition to the C(S) response type - two types of C(T) responses and the O(C) type. The different patterns of firing regularity exhibited by C(S/T) neurons reflected different thresholds or degrees of overlap between these cells' narrowly tuned excitatory and inhibitory inputs. C(T) cells with closely matched inhibitory and excitatory response areas showed substantial on-CF inhibition and the greatest decline in firing regularity during a CF tone, whereas those with a mismatch between their response areas showed lateral inhibition and a less marked decline in firing regularity. The presence of inhibition in C(S) neurons did not alter their firing regularity, possibly because of the lower threshold for excitation compared with inhibition. The latency, duration and frequency extent of sustained hyperpolarization in C(S/T) cells is inconsistent with the response properties of O(C) neurons, suggesting that another source(s) of inhibition influences firing regularity, and presumably response magnitude, in these neurons.

Fast inhibition alters first spike timing in auditory brainstem neurons.

Within the first processing site of the central auditory pathway, inhibitory neurons (D stellate cells) broadly tuned to tonal frequency project on narrowly tuned, excitatory output neurons (T stellate cells). The latter is thought to provide a topographic representation of sound spectrum, whereas the former is thought to provide lateral inhibition that improves spectral contrast, particularly in noise. In response to pure tones, the overall discharge rate in T stellate cells is unlikely to be suppressed dramatically by D stellate cells because they respond primarily to stimulus onset and provide fast, short-duration inhibition. In vivo intracellular recordings from the ventral cochlear nucleus (VCN) showed that, when tones were presented above or below the characteristic frequency (CF) of a T stellate neuron, they were inhibited during depolarization. This resulted in a delay in the initial action potential produced by T stellate cells. This ability of fast inhibition to alter the first spike timing of a T stellate neuron was confirmed by electrically activating the D stellate cell pathway that arises in the contralateral cochlear nucleus. Delay was also induced when two tones were presented: one at CF and one outside the frequency response area of the T stellate neuron. These findings suggest that the traditional view of lateral inhibition within the VCN should incorporate delay as one of its principle outcomes.

Ventral cochlear nucleus coding of voice onset time in naturally spoken syllables.

These experiments examined the coding of the voice onset time (VOT) of six naturally spoken syllables, presented at a number of intensities, by ventral cochlear nucleus (VCN) neurons in rats anesthetized with urethane. VOT is one of the cues for the identification of a stop consonant, and is defined by the interval between stop release and the first glottal pulse that marks the onset of voicing associated with a vowel. The syllables presented (/bot/, /dot/, /got/, /pot/, /tot/, /kot/) each had a different VOT, ranging between 10 and 108 ms. Extracellular recordings were made from single neurons (N=202) with a wide range of best frequencies (BFs; 0.66-10 kHz) that represented the major VCN response types - primary-like (67.8% of sample), chopper (19.8%), and onset (12.4%) neurons. The different VOTs of the syllables were accurately reflected in sharp, precisely timed, and statistically significant changes in average discharge rate in all cell types, as well as the entire VCN sample. The prominence of the response to stop release and voice onset, and the level of activity prior to the VOT, were influenced by syllable intensity and the spectrum of stop release, as well as cell BF and type. Our results suggest that the responses of VCN cells with BFs above the first formant frequency are dominated by their sensitivity to the onsets of broadband events in speech, and allows them to convey accurate information about a syllable's VOT.