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)