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Target-Ranging Theories
spectrogram correlation process is capable of achieving delay accuracies comparable to a matched filter, but the properties of delay-tuned neurons created by this mechanism do not appear to be the vehicle for achieving the bat’s actual perfor- mance (Pollak, 1980). How is this difference to be explained?
The obvious place to look is at the timing of the spikes instead of the delay-tuning curves themselves. Although delay tun- ing is manifested in milliseconds, the latencies of the spikes vary by only a few hundred microseconds in most cells, a re- duction in timing errors of up to 100 times (Simmons et al., 1996). Figure 4C shows the delay lines for spectrogram cor- relation just schematically and very qualitatively, whereas the actual numerical values of the spike latencies, the phasic-on responses that constitute the delay taps, are arranged period- ically at intervals of about 2 to 3 milliseconds (Simmons and Simmons, 2010). This periodicity is present in the latencies of responses evoked by both broadcasts and echoes (Simmons et al., 1996). Its presence points to underlying oscillatory sig- nals in the representation of the broadcasts and echoes that provides a way for fine delay changes to affect how these os- cillatory signals interact and interfere with each other. These oscillations suggest that a neural heterodyning process may be manifested in the inferior colliculus and its subsequent neuronal circuits to register small, microsecond-scale chang- es in echo delay as shifts in interference patterns across the time (i.e., latency) dimension. This would render seemingly microscopic changes in echo delay into large changes in re- sponse probability and latency that would be recognizable by the much more sluggish responses of neurons. The hallmark of a vernier-like interference process is the magnification of small changes in timing into larger changes in the product of the interference, which has been observed in big brown bats (Simmons et al., 1996). This mechanism may explain the big brown bats extraordinary submicrosecond sensitivity to changes in echo delay.
Implications for Hearing in General
The periodic organization of single-spike on-response laten- cies and their role in registering the timing of sounds are not restricted to big brown bats; it is present, too, in the inferior colliculus of bullfrogs and of cats (Simmons and Simmons, 2010). The auditory cortex, at the top of the auditory pro- cessing pathway, is thought of as a display of information for perception, but it also feeds information back to the integrat- ing center of the inferior colliculus, which is responsible for the distributed nature of spike latencies. The time lags asso-
ciated with this excitatory feedback may produce the peri- odic pattern of latencies, which maybe critical for the fine perception of echo delay. This, in turn, means that the con- cepts of display and processing are intermingled across levels in the auditory system, which raises the possibility that the superior performance echolocation may require radical new technology to replicate.
The computational studies for this article were supported by Office of Naval Research Grant N00014-14-1-05880. I am grateful for the assistance of the Acoustics Today editor in preparing this work.
Jim Simmons was an undergraduate at Union Junior College in New Jersey and Lafayette College in Pennsylvania. He was a graduate student of E. G. Wever at Princeton University where he began working with echolocating bats. He taught at Washington University in St.
Louis for 10 years, where his colleagues were Nobuo Suga and the many members of the auditory community at the Central Institute for the Deaf. He moved to the University of Oregon for four years as part of a group of neuroetholo- gists and has been at Brown University since 1985 in psy- chology and then in neuroscience.
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Neuweiler, G. (2000). The Biology of Bats. Oxford University Press, New York. Pollak, G. D. (1980). Organizational and encoding features of single neu- rons in the inferior colliculus of bats. In Busnel, R.-G., and Fish, J. F. (Eds.),
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