Neural representation of target distance in auditory cortex of the echolocating bat Myotis lucifugus

Abstract

1. Single- and multiunit recordings were obtained from neurons in the auditory cortex of the echolocating bat Myotis lucifugus, while trains of stimuli designed to simulate the bat's frequency-modulated (FM) orientation pulse and its returning echo were delivered. It was found that many neurons in the cortex responded selectively to pulse-echo pairs only if the time delay separating the artificial pulse and the echo was within a certain range. This response property is called "delay-dependent facilitation." Since echolating bats are known to utilize echo-delay information for the determination of target distance, it is postulated that these neurons are involved in the process of distance perception. 2. Two types of delay-sensitive neurons were characterized on the basis of their response patterns. P-type units had short maximum response delays, narrow delay response functions, and response latencies for pulse-echo pairs that were similar to their response latencies for single loud FM pulses. E-type units had longer maximum response delays, wide delay response functions, and pulse-echo pair response latencies that were time-locked to the echo. Another important difference between these two classes was that changes in the amplitude of the artificial echo caused systematic changes in the delay response of E-type units but not of P-type units. 3. The sharpness and stability of the delay response functions of P-type units suggested that they may encode target distance by responding at discrete echo delays. In contrast, delay tuning may not be an unambiguous determinant of echo delay in E-type units. Here, the most consistent and reliable response parameter for echo delay is the time at which the responses occurred. This suggested that echo delay could be encoded by the temporal pattern of responses in E-type units in relation to the responses evoked by the outgoing orientation cry. The different range of delay of delay sensitivity of P-type and E-type units indicates that these two mechanisms could be operating at different ranges of target distance. 4. P-type and E-type responses may not be due to different populations of neurons but to different response properties of the same population under different conditions. Evidence for this proposition was obtained by showing that in some recordings, decreases in the amplitude of the artificial pulse caused a switch in response from a long best delay, E-type response to a short best delay, P-type response. This suggested that the delay sensitivity of cortical neurons could be under the bat's control based on the intensity of its pulse emissions.

Spatially Selective Auditory Responses in the Superior Colliculus of the Echolocating Bat

“…The small shift in the average latency follows the time-intensity trading relationship described for most other auditory neurons, with a stronger sound evoking a discharge with a shorter latency than a weaker sound (Pollak, 1988;Simmons et al, 1990;Burkard and Moss, 1994). No evidence of paradoxical latency shifts in 3D neurons was observed (see Sullivan, 1982), i.e., the response latency to the stronger pulse was not delayed with respect to the response latency to the weaker echo.…”

“…The latency of the neural response was corrected for the time delay for the signal to travel the distance from the speaker to the ears of the bat and for the delay imposed by the synchronization signal to the data acquisition system, totaling a correction factor of 6.48 msec subtracted from the response latencies. For units that exhibited echo-delay facilitation, the latency of the neural response was expressed in two ways: from the onset of the first stimulus in the pair (pulse facilitation latency, PFL), and from the onset of the second stimulus (echo facilitation latency, EFL) (Sullivan, 1982;Dear et al, 1993b). The timing of impulses with respect to stimulus onset is demonstrated in the raster-dot display of Figure 3A for activity recorded from a single cell in response to a fixed delay stimulus.…”

Evolution of high duty cycle echolocation in bats

“…These are delay-tuned and duration-tuned neurons. Delaytuned neurons are found in the inferior colliculus and cortex of both LDC and HDC bats, and are thought to be important for extracting information about target range/distance (O'Neill and Suga, 1979;Sullivan, 1982;Schuller et al, 1991;Casseday et al, 1994;Yan and Suga, 1996;Galazyuk and Feng, 1997;Portfors and Wenstrup, 1999). Delay-tuned neurons show a facilitated response and fire maximally when the timing (delay) between two sounds -the outgoing pulse and returning echo -corresponds to the cell's best delay.…”

Activation of the serotonin 1A receptor alters the temporal characteristics of auditory responses in the inferior colliculus

“…Thus, long-latency neurons create delay lines for stimulus features occurring earlier in time that must converge with short-latency lines for stimulus features occurring later in time, in order to generate a maximal response. In bat inferior colliculus, such delay lines are proposed to be involved in encoding stimulus features such as the delay between an echolocation call and its returning echo (O'Neill and Suga, 1982;Sullivan, 1982;Berkowitz and Suga, 1989;Dear et al, 1993;Mittmann and Wenstrup, 1995;Wenstrup et al, 1999;Portfors and Wenstrup, 1999), or the duration of a sound, through the appropriate coincidence of onset and offset responses Ehrlich et al, 1997;Faure et al, 2003). The current results suggest that for both of these temporal coding models, activation of 5-HT 1A receptors would disproportionately disrupt the representation of the longest or most widely spaced features of sound by suppressing the responses of proportionally more longer-latency neurons.…”

“…Such a one-way correlation would also be suggestive of the function of the 5-HT 1A receptor, since variation along the axis of each of these three characteristics carries functional implications. For example, neurons in dorsal versus ventral IC are differentially involved in triggering aversive behaviors (Ferreira-Netto et al, 2007), neurons with different CFs respond best to complex vocalizations with different spectra (Klug et al, 2002), and neurons with different latencies may encode different temporal features of sound (O'Neill and Suga, 1982;Sullivan, 1982;Langner et al, 1987;Langner and Schreiner, 1988;Berkowitz and Suga, 1989;Dear et al, 1993;Hopfield, 1995;Langner et al, 2002).…”