Midbrain auditory selectivity to natural sounds

Melville J. Wohlgemuth; Cynthia F. Moss

doi:10.1073/pnas.1517451113

New Research In

Edited by Jon H. Kaas, Vanderbilt University, Nashville, TN, and approved January 21, 2016 (received for review September 10, 2015)

Significance

Nervous systems have evolved to enable processing of complex stimuli that animals encounter in their natural environments, and yet, neurophysiological research has largely investigated responses to simple artificial stimuli. In an attempt to bridge this gap, we characterized response selectivity to natural stimuli in the midbrain superior colliculus (SC) of the echolocating bat, an animal that probes the environment with sonar vocalizations. Using the bat’s dynamic echolocation signals as auditory stimuli, we discovered that SC neurons in the dorsal sensory layers exhibited selectivity that was not predicted by responses to artificial sounds. Our research reveals how response properties of SC auditory neurons may lead to stimulus selection and further shows the importance of biologically relevant stimuli to understand brain function.

Abstract

This study investigated auditory stimulus selectivity in the midbrain superior colliculus (SC) of the echolocating bat, an animal that relies on hearing to guide its orienting behaviors. Multichannel, single-unit recordings were taken across laminae of the midbrain SC of the awake, passively listening big brown bat, Eptesicus fuscus. Species-specific frequency-modulated (FM) echolocation sound sequences with dynamic spectrotemporal features served as acoustic stimuli along with artificial sound sequences matched in bandwidth, amplitude, and duration but differing in spectrotemporal structure. Neurons in dorsal sensory regions of the bat SC responded selectively to elements within the FM sound sequences, whereas neurons in ventral sensorimotor regions showed broad response profiles to natural and artificial stimuli. Moreover, a generalized linear model (GLM) constructed on responses in the dorsal SC to artificial linear FM stimuli failed to predict responses to natural sounds and vice versa, but the GLM produced accurate response predictions in ventral SC neurons. This result suggests that auditory selectivity in the dorsal extent of the bat SC arises through nonlinear mechanisms, which extract species-specific sensory information. Importantly, auditory selectivity appeared only in responses to stimuli containing the natural statistics of acoustic signals used by the bat for spatial orientation—sonar vocalizations—offering support for the hypothesis that sensory selectivity enables rapid species-specific orienting behaviors. The results of this study are the first, to our knowledge, to show auditory spectrotemporal selectivity to natural stimuli in SC neurons and serve to inform a more general understanding of mechanisms guiding sensory selectivity for natural, goal-directed orienting behaviors.

Footnotes

↵¹Present address: Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD 21218.
↵²To whom correspondence should be addressed. Email: melville.wohlgemuth{at}jhu.edu.

Author contributions: M.J.W. designed research; M.J.W. performed research; M.J.W. analyzed data; and M.J.W. and C.F.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1517451113/-/DCSupplemental.

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