Encoding of target range and its representation in the auditory cortex of the mustached bat

Abstract

The time course of acoustic events is a critical element for the recognition of biologically rneaningful sounds. Echolocating bats analyze the time intervals between their emitted biosonar pulses and the echoes returning from objects to assess target distance (range). In this study, we have explored the auditory cortex of the mustached bat, Pteronotus parnellii rubiginosus, using pairs of acoustic stimuli mimicking the multiharmonic biosonar signals (pulses) used by this species and their echoes.A discrete field of auditory cortex dorsorostral to the tonotopicaJly organized primary field contains neurons which are insensitive to pure tone, frequency-modulated (FM), or noise stimuli presented singly. Rather, they respond strongly to pairs of stimuli, specifically, the fundamental FM component of the pulse paired with an FM component of one of the higher harmonics of the echo. We call these neurons FM1-FM, facilitation neurons. There are three separate longitudinal clusters in this cortical area containing FM1-FM2, FM1-FM3, and FMI-FM4 neurons, respectively. Moreover, FMI-FM, neurons are specifically sensitive to the time delay between the two FM components, i.e., the time delay of the echo from the pulse. Thus, they can decode target range.Two types of delay-sensitive neurons were found. Tracking neurons, whose response to echo delay varied according to repetition rate and stimulus duration, were found rarely. Delay-tuned neurons, which were tuned to specific time delays (best delays) of the echo from the pulse, were much more evident. Both types of neurons are organized into columns with similar best delays, and the best delay of delay-tuned neurons was found to increase systematically along the cortical surface in the rostrocaudal direction. This area, therefore, contains a neural representation of target range along this best delay axis. Such an axis exists in each of the clusters of FMI-FMz, FM]-FM3, and FMI-FM4 neurons. This is a new type of cortical organization which is not tonotopic but which represents an important acoustic cue related to the time course of acoustic events. Acoustic signals can be described in terms of physical parameters, such as frequency, amplitude, and time. time to convey information. Although the temporal patterns within phonemes and their sequences in the acoustic stream carry much of the total information in vocalizations, research in mammalian audition has focused mainly on the analysis and representation of frequency in the auditory system. That the cochlea is primarily a frequency analyzer (von B6k6sy, 1960) probably accounts for much of this emphasis. Another factor in favor of this bias is the relative ease of generation and the physical simplicity of pure tone stimuli for investigating the properties of the auditory system. A major result of this endeavor has been to show that central auditory organization is dominated by the recapitulation of the morphology of the sensory epithelium, i.e., the organ of Corti. Mapping of peripheral organization onto the central ner...

Auditory cortex of newborn bats is prewired for echolocation

“…For all age groups, CP was 2-6 dB more sensitive than PP (days 0-7: 64 ± 15 dB SPL; days 20-28: 54 ± 12 dB SPL; adult: 44 ± 9 dB SPL). The data for anaesthetized adult PP are comparable to published data on awake bats 3,6,7,16,17 . The threshold decrease of neurons that were grouped into short, medium and long CD units (Fig.…”

“…In the neonates, cortical regions that would correspond to the caudal FM-FM area in adults were not responsive to pure tones or FM-FM pairs. As in the adult ventral FM-FM region 3 , the neurons responded best to stimulus pairs containing a second harmonic FM E . In CP, developmental changes of chronotopy could be studied by pooling data from a number of animals that were of the same age within ± 1 day (Fig.…”

“…Short downward frequency-modulated (FM) sweeps are used as echolocation calls or call components in all bat species known. The FM signal serves two purposes: it provides information about target surface structure based on spectral changes in the echo and it is used as time marker to allow a precise neuronal calculation of target distance from echo delay [1][2][3][4][5] .…”

“…As a neuronal correlate for target distance calculation, neurons in the auditory cortex (AC) of echolocating bats have been described that selectively respond to pairs of FM stimuli that represent pulse and echo 3,[6][7][8][9][10] . These combination-sensitive neurons are maximally facilitated at specific delays between pulse and echo.…”

“…The extraction of target distance from echo delay is a purely computational feature established in the ascending auditory system of bats, that unlike frequency tuning, does not directly depend on the receptor surface in the inner ear 3,7,9 . Therefore, we expected that its neuronal implementation would require periods of experiencedependent plasticity during postnatal development.…”