Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation

Abstract

1. The biosonar signal (pulse) of the mustached bat, Pteronotus parnellii parnellii, has four harmonics (H1-4), each consisting of a long constant-frequency component (CF1-4) followed by a short frequency-modulated component (FM1-4). As the bat approaches a target, it systematically modifies its pulses to optimize the extraction of information from the echoes. These behavioral responses include 1) Doppler-shift (DS) compensation in which the bat adjusts the frequency of its pulses to correct for the DS in the echoes. This maintains the echo CF2 at a frequency to which the bat's cochlea is very sharply tuned, slightly above the CF2 frequency of the bat's pulses when it is at rest (Frest, approximately 61 kHz); 2) echo intensity compensation, in which the bat lowers its pulse intensity as it approaches a large target, thus maintaining the echo intensity within a suitable range for auditory processing; and 3) and 4) duration and rate adjustments, in which the bat first increases its pulse duration to facilitate target identification, then shortens its pulse duration while increasing its pulse rate to facilitate target analysis. 2. We examined these responses, especially DS compensation, by swinging bats on a pendulum toward a large target over a distance of 3.6 m. Eight bats were given 15-30 swings per day for 6-25 days. 1) On 97% of all swings the bats showed strong DS compensation as the pendulum approached the target. They did not show DS compensation on the backswing. 2) On 40-50% of all swings, the bats clearly displayed the other responses. The bats typically increased their pulse intensity a small amount early in the pendulum swing, then decreased pulse intensity by as much as 18 dB as the target was more closely approached. They increased their pulse intensity during the backswing. 3) Pulse duration increased from approximately 20 to 23 ms early in the forward swing, decreased to approximately 18 ms as the target was more closely approached, and then increased to 20 ms by the end of the backswing. 4) The instantaneous repetition rate increased from approximately 17 pulses/s at the start of the forward swing to approximately 28 pulses/s near the target, then decreased to approximately 10 pulses/s by the end of the backswing. Pulses usually occurred in trains of 1-2 pulses, with longer trains occasionally occurring near the target. 3. The maximum DS on the pendulum was 1.34 kHz, and the maximum DS compensation was 146 +/- 98 (SD) Hz less than this value.(ABSTRACT TRUNCATED AT 400 WORDS)

A Neural Basis for Auditory Feedback Control of Vocal Pitch

“…This network potentially includes several midbrain structures, such as the superior colliculus, the periaqueductal gray, and areas laterally and ventrally adjacent to the periaqueductal gray (Suga et al, 1973;Jürgens and Pratt, 1979;Larson and Kistler, 1986;Rübsamen and Betz, 1986;Thoms and Jürgens, 1987;Schuller and Radtke-Schuller, 1990;Kirzinger and Jürgens, 1991;Larson, 1991;Jürgens and Lu, 1993;Gerrits and Holstege, 1996;Schuller et al, 1997;Jürgens, 1998Jürgens, , 2000Jürgens, , 2002Behrend and Schuller, 2000). This midbrain network can function independently from higher-order structures of vocalization control, such as the cingulate cortex (Movchan and Burikova, 1982;Movchan, 1984;Gaioni et al, 1990;Riquimaroux et al, 1992), and lesions at the level of the midbrain dramatically affect sound production in various mammals (Movchan, 1980;Movchan and Burikova, 1982;Kirzinger and Jürgens, 1985;Schuller, 1986;Konstantinov et al, 1988;Jürgens, 1998Jürgens, , 2002. Previously, oftenneglected studies in horseshoe bats suggested that after bilateral ablation of the deep layers of the inferior colliculus and ventrally adjacent portions of the tegmentum including PB, call frequencies emitted at rest and during DSC became less stable and eliminated DSC behavior or even "inverted" the response; instead of decreasing its vocalization frequency in response to increasing echo frequencies, the bat's vocalization frequency increased on average 1 kHz above RF (Movchan, 1984;Konstantinov et al, 1988).…”

“…In 3 of the 14 animals, we also tested the effects of the drugs on compensation behavior to natural Doppler-shifted echoes in bats that were swung on a pendulum against a large echo target (Gaioni et al, 1990). For this purpose, the bats are placed in a body mold made from soft foam and attached to the base of the pendulum immediately after the end of drug injections and the injection pipettes had been retracted from the brain.…”

“…To examine whether the bats failed to show DSC behavior after drug injections merely because these agents affected the motivational state of the animal, thus masking DSC, we also tested the compensation behavior after drug injection while the bat was swinging on a pendulum against a large background target (Gaioni et al, 1990). (Note that the injection pipettes had been retracted, and the animal had been removed from the experimental setup used to test for artificially frequency-shifted echo mimics; for details, see Materials and Methods.)…”

The sense of touch in the star-nosed mole: from mechanoreceptors to the brain

“…The existence of a tactile fovea in the star-nosed mole can be compared with the well-known retinal fovea in other mammals, and also with the acoustic fovea of bats. Moustached bats have a well-characterized acoustic fovea evident from the level of the cochlea [43] to the auditory cortex [44], and Doppler shift compensation behaviour [45] can be considered functionally equivalent to a foveation movement. The existence of a foveaperiphery division of sensory surfaces in the visual, auditory and somatosensory systems of different mammals suggests that this organizational scheme is an efficient general solution to producing a very highresolution sensory system.…”

Sensory feedback control of mammalian vocalizations

“…However, within the bat's ascending auditory system, single neuron response latencies in the range of 20-25 ms appear as early as the midbrain inferior colliculus [97], which makes it hard to imagine that any more sophisticated and time-consuming cortical processing might be involved in the DSC behavior. Electrical stimulations of the mustached bat anterior cingulate cortex evoked echolocation calls that varied in call frequency over the same range of frequencies as those utilized during DSC [36,37], yet surgical ablation of the so-called "DSC region" of the auditory cortex did not prevent the bats from performing DSC [34]. Where then is the main connection between the ascending auditory and descending vocal motor systems guiding the automated stabilization of echo frequencies?…”