Many acoustic communication signals, including human speech and music, consist of a precise temporal arrangement of discrete elements, but it is unclear whether this precise temporal patterning is required to activate the sensory neurons that mediate signal recognition. In a variety of systems, neurons respond selectively when two or more sound elements are presented in a particular temporal order and the precise relative timing of these elements is particularly important for 'delay-tuned' neurons, including 'tracking' types, in bats. Here we show that one class of auditory neurons in the midbrain of anurans (frogs and toads) responds only to a series of specific interpulse intervals (IPIs); in the most selective cases, a single interval that is slightly longer or shorter than the requisite interval can reset this interval-counting process.

This study examined the mechanisms underlying amplitude modulation selectivity in the anuran auditory midbrain. Single units were recorded extracellularly in the torus semicircularis of the northern leopard frog, Rana pipiens. Two physiologically distinct classes of neurons were identified, based on their response latencies and their selectivities to pulse repetition rates. Cells in one group had short response latencies (median = 31 ms) and responded best to pulse repetition rates below 40 Hz. Tuning to low amplitude modulation rates was largely determined by recovery processes and phasic response properties. Cells in the second group had much longer latencies (median=81 ms) and were generally selective for pulse repetition rates greater than 40-50 Hz. Sensitivity to higher amplitude modulation rates resulted from integration processes; these units only responded when a threshold number of pulses were presented at a minimum pulse density (amplitude modulation rate). At amplitude modulation rates above their best rate, their responses decreased, apparently due to inadequate recovery time between pulses.

Analysis of the temporal structure of acoustic signals is important for the communication and survival of a variety of animals including humans. Recognition and discrimination of particular temporal patterns in sounds may involve integration of auditory information presented over hundreds of milliseconds or seconds. Here we show neural evidence for long-term integration in the anuran auditory system. The responses of one class of auditory neurons in the torus semicircularis (auditory midbrain) of frogs reflect the integration of information, gathered over approximately 45-150 ms, from a series of stimulus pulses, not stimulus energy. This integration process is fundamental to the selective responses of these neurons for particular call types.

Edwards, Christofer J., Todd B. Alder, and Gary J. Rose. Pulse rise time but not duty cycle affects the temporal selectivity of neurons in the anuran midbrain that prefer slow AM rates. J Neurophysiol 93: 1336 -1341, 2005; doi:10.1152/jn.00797.2004. Recovery-type auditory neurons in the anuran inferior colliculus (IC) respond with band-pass or low-pass selectivity for sinusoidal AM. These cells respond to each modulation cycle at slow AM rates and respond only at the onset of fast AM or pulse repetition rate (PRR) stimuli, failing to recover from the effects of early pulses. This selectivity is not altered by changes in pulse duty cycle. The recovery process is governed therefore by the interpulse interval and not the dimension of the gap between sound pulses. Most of these neurons preferred fast rise times, which is characteristic of the sound pulses in the calls of Hyla regilla and Rana pipiens, the two species selected for this study.

The weakly electric fish, Eigenmannia, changes its frequency of electric organ discharges (EODs) to increase the frequency difference between its EODs and those of a jamming neighbor. This jamming avoidance response is greatest for frequency differences (i.e., beat rates) of approximately 4 Hz and barely detectable at beat rates of 20 Hz. A neural correlate of this behavior is found in the torus semicircularis, where most neurons act as low-pass or band-pass filters over this range of beat rates.This study examines two mechanisms that could possibly underlie low-pass temporal filtering: 1) Inhibition by a 'high-pass' interneuron. 2) Voltage and time-dependent conductances associated with ligand-gated channels. These mechanisms were tested by recording intracellularly while employing stimuli consisting of simultaneous low and high beat rates. A neuron's response to the low beat rate was not diminished by the addition of the higher frequency jamming signal (thereby superimposing a high rate of amplitude and phase modulation onto the lower rate), and the 'inhibitory interneuron' hypothesis is, therefore, not supported. Also, the responses to the high beat rate were not facilitated during maintained depolarization in response to the low beat rate.In some cases, particularly band-pass neurons, accommodation processes appeared to contribute to the decline in the amplitude of psps at high beat rates.