Temporally selective processing of communication signals by auditory midbrain neurons

Perception of the temporal structure of acoustic signals contributes critically to vocal signaling. In the aquatic clawed frog Xenopus laevis, calls differ primarily in the temporal parameter of click rate, which conveys sexual identity and reproductive state. We show here that an ensemble of auditory neurons in the laminar nucleus of the torus semicircularis (TS) of X. laevis specializes in encoding vocalization click rates. We recorded single TS units while pure tones, natural calls, and synthetic clicks were presented directly to the tympanum via a vibration-stimulation probe. Synthesized click rates ranged from 4 to 50 Hz, the rate at which the clicks begin to overlap. Frequency selectivity and temporal processing were characterized using response-intensity curves, temporal-discharge patterns, and autocorrelations of reduplicated responses to click trains. Characteristic frequencies ranged from 140 to 3,250 Hz, with minimum thresholds of −90 dB re 1 mm/s at 500 Hz and −76 dB at 1,100 Hz near the dominant frequency of female clicks. Unlike units in the auditory nerve and dorsal medullary nucleus, most toral units respond selectively to the behaviorally relevant temporal feature of the rate of clicks in calls. The majority of neurons (85%) were selective for click rates, and this selectivity remained unchanged over sound levels 10 to 20 dB above threshold. Selective neurons give phasic, tonic, or adapting responses to tone bursts and click trains. Some algorithms that could compute temporally selective receptive fields are described.

Heterogeneous Biophysical Properties of Frog Dorsal Medullary Nucleus (Cochlear Nucleus) Neurons

The cochlear nucleus (CN) in mammals, or its counterpart in birds, has multiple subdivisions each containing distinct morphological and functional (i.e., temporal discharge patterns and biophysical properties) cell types that project to different auditory nuclei in the brain stem in parallel. The analogous structure in frogs, the dorsal medullary nucleus (DMN), is a single phylogenetically older structure with no subdivision. Similar to the CN, the DMN has complex cytoarchitecture and contains neurons with diverse morphological phenotypes, but whether these cell types possess distinct biophysical characteristics, like their counterparts in mammals and avians, is unclear. Here we show that DMN neurons in young adult northern leopard frogs ( Rana pipiens pipiens) possess heterogeneous biophysical properties. There are four major biophysical phenotypes on the basis of the unit's response (i.e., its temporal firing pattern) to depolarizing currents: onset, phasic-burst, sustained-chopper, and adapting. These cells have distinct membrane input resistances and time constants, spike shapes, current-voltage relationships, first-spike latencies, entrainment characteristics, and ionic compositions (i.e., low-threshold potassium current, Ikl, and hyperpolarization-activated current, Ih). Furthermore, these phenotypes correspond to cells' dendritic morphologies, and they bear similarities and differences to those found in the mammalian CN. The similarities are remarkable considering that amphibians are a distinct evolutionary lineage from birds and mammals.

Temporal processing in the dorsal medullary nucleus of the Northern leopard frog (Rana pipiens pipiens)

1. Single-unit responses to different temporal acoustic parameters were characterized in the dorsal medullary nucleus (DMN) of the Northern leopard frog, Rana pipiens pipiens. Our goal was to provide both a quantitative and a qualitative assessment of the neural representation of behaviorally relevant temporal acoustic patterns in the frog's DMN. 2. Acoustic stimuli included tone bursts having different durations, rise times, or rates of amplitude modulation (AM). Several metrics were used to compute temporal response functions for each of these, including mean spike count, average firing rate, and/or peak firing rate. Synchronization coefficients were also used to characterize responses to stimuli presented at different AM rates. 3. On the basis of mean spike count, the temporal response functions of DMN neurons with respect to signal rise time could be characterized as 1) all-pass, in which the mean spike count was largely independent of rise time, or 2) fast-pass, in which the mean spike count decreased with increasing rise time. Fast-pass response functions were of two types, those that decayed rapidly and those that decayed gradually from their peak values. 4. The minimum threshold varied with signal rise time for cells showing fast-pass but not all-pass response functions. Minimum response thresholds for fast-pass neurons were typically higher with slower signal rise time. 5. The filtering characteristics of cells displaying fast-pass rise time response functions were dependent on signal level, becoming all-pass when signal levels exceeded 30-40 dB above the minimum threshold. 6. Approximately 44% of DMN neurons exhibiting fast-pass response functions for signal rise time showed all-pass filtering characteristics when broadband noise rather than best frequency tones were used, thereby signifying an influence of signal spectrum on the pass-band characteristics of these cells. 7. All DMN neurons, regardless of discharge pattern, showed maximal instantaneous firing rates to signals having short (less than 25 ms) rise times. Response functions based on instantaneous firing rate were, therefore, fast-pass in nature. These responses were independent of signal level and spectrum. 8. There was an ordinal relationship between signal duration and the duration of tonic but not phasic unit discharges. This relationship was not intensity dependent. 9. On the basis of mean spike count, the temporal response functions of DMN neurons with respect to signal duration were characterized as 1) all-pass, in which the mean spike count was largely independent of signal duration, or 2) long-pass, in which the mean spike count increased with increasing signal duration.(ABSTRACT TRUNCATED AT 400 WORDS)

Classification of the temporal discharge patterns of single auditory neurons in the dorsal medullary nucleus of the northern leopard frog

1. The dorsal medullary nucleus (DMN) of frogs is the presumed homolog of the mammalian cochlear nucleus (CN). Like the CN, the DMN is the sole target of centrally projecting primary auditory-nerve fibers and the first central auditory-processing center. To study the transformation of acoustic information in the DMN, we have utilized relatively simple stimuli--tone bursts--to detail the temporal discharge patterns of DMN neurons that can be compared with those shown by auditory-nerve fibers. 2. Based on the shape of poststimulus time (PSTH) and interspike interval (ISIH) histograms, we observed six distinctive discharge patterns to tone bursts presented at the best excitatory frequency (BEF), 10 dB above threshold. Four of these (primary-like type 1-4) resembled discharge patterns seen at the level of the auditory nerve, whereas two (phasic and phasic burst) were only observed in the DMN. 3. At stimulus levels of 20-30 dB above BEF threshold several phasic neurons became tonic responders, whereas several primary-like type-2 cells gave "pauser" discharges. The response patterns of the remaining cells were intensity independent. 4. We further showed that many of the single-unit discharge patterns were related to other neuronal response properties; specifically, spontaneous firing rate, intensity-rate functions, threshold, latency, BEF, and sharpness of tuning (Q10). 5. The implications of our findings are discussed with respect to 1) the transformation of acoustic information as it is passed from the auditory nerve to the DMN, and 2) the functional organization of the DMN.

Reorganization of connectivity in amphibian central auditory system following VIIIth nerve regeneration: time course

In the frog, most neurons in the primary (dorsal medullary nucleus, DMN) and secondary (superior olivary nucleus, SO) auditory nuclei have V-shaped tuning curves, almost as narrowly tuned as those recorded in the nerve. Thus, the innervation pattern is such that if more than one excitatory afferent innervates a postsynaptic cell, they must all possess similar best frequencies (BFs). Similarly, binaural cells in these nuclei display matched frequency selectivities when acoustically stimulated via either ear. The VIIIth nerve was unilaterally severed and allowed to regenerate back into the DMN. At various postoperative intervals, extracellular single-unit recordings were made in the SO contralateral to the regenerated nerve, as that nucleus receives its dominant excitatory input (approximately 80%) from the contralateral side. Recordings were also made in the SO of a number of unoperated control animals. Functional reinnervation commenced between 4 and 5 wk postoperatively and by 6 wk, a normal innervation density, as judged by physiological criteria, was achieved. Single units of any best frequency represented within the frog's two auditory papillae could be recorded during earliest reinnervation. In general, the tuning curves of both monaural and binaural cells were V shaped in the 6 wk regenerates. Although many tuning curves were narrowly tuned (Q10dB greater than 1.0) as in unoperated animals, some were very broadly tuned (Q10dB less than 0.5). The mean Q10dB value for all contralaterally excited cells was 1.45 +/- 0.77 (SD), which was significantly lower than that of SO units in unoperated frogs (Q10dB = 1.66 +/- 0.52 (SD)). Binaural cells often had mismatched BFs and tuning curves. By 8 wk after nerve transection, tuning curves were as narrow as in unoperated animals (Q10dB = 1.64 +/- 0.68 (SD)), and the BFs of binaural cells evinced a greater match than at 6 wk. By 12 wk postoperatively, V-shaped tuning curves were still as narrow as in controls (Q10dB = 1.71 +/- 0.69 (SD)), and the tuning curves and BFs of binaural cells were well matched again. At all postoperative intervals, about 10% of the tuning curves in the SO of regenerates were W shaped. This was never seen in normal animals. The return of narrow V-shaped tuning curves in the majority of neurons and the recurrence of matched binaural cells in the SO are interpreted as evidence of specificity for potential postsynaptic targets in the DMN by regenerating auditory afferents.