Midbrain auditory selectivity to natural sounds

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, singleunit recordings were taken across laminae of the midbrain SC of the awake, passively listening big brown bat, Eptesicus fuscus. Speciesspecific 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 vocalizationsoffering 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.stimulus selection | superior colliculus | auditory grasp | neuroethology

Processing of Natural Echolocation Sequences in the Inferior Colliculus of Seba’s Fruit Eating Bat,Carollia perspicillata

“…5 ). In agreement with our results, numerous studies have reported that subcortical neurons sharpen their neuronal tuning with increasing repetition rates [IC: Myotis lucifugus ( Friend et al, 1966 ; Galazyuk et al, 2000 ), E. fuscus ( Pinheiro et al, 1991 ; Chen and Jen, 1994 ; Moriyama et al, 1994 ; Wu and Jen, 1996 ; Jen and Chen, 1998 ; Jen and Zhou, 1999 ; Jen et al, 2001 ; Zhou and Jen, 2001 ; Zhou and Jen, 2002 ; Sanderson and Simmons, 2005 ; Wu and Jen, 2006 ; Zhou and Jen, 2006 ; Jen and Wu, 2008 ); superior colliculus: E. fuscus ( Valentine and Moss, 1997 ; Wohlgemuth and Moss, 2016 )]. Some studies even described repetition rate selective neurons in the IC of insectivorous bats, like E. fuscus , ( Pinheiro et al, 1991 ; Sanderson and Simmons, 2005 ) and M. lucifugus ( Condon et al, 1994 ).…”

“…Thus, to understand the neuroethological roles of the auditory centers involved in processing echolocation signals, it is necessary to investigate neuronal processing with natural echolocation sequences. So far, processing of natural echolocation sequences has been characterized in the superior colliculus of the insectivorous bat Eptesicus fuscus ( Wohlgemuth and Moss, 2016 ) and in the auditory cortex (AC) of C. perspicillata ( Beetz et al, 2016a , b ). Cortical results have shown that the natural temporal context evokes neuronal suppression which results into a high neuronal selectivity to particular call echo pairs ( Beetz et al, 2016a ) or to object-specific echo information ( Beetz et al, 2016b ).…”

Temporal tuning in the bat auditory cortex is sharper when studied with natural echolocation sequences

“…Based on these differences, one could argue that suppression effects could be stronger when studied with natural (as opposed to seminatural) echolocation sequences. Supporting this idea, a recent electrophysiological study showed stronger selectivity to natural than to artificial echolocation streams in subcortical neurons of the big brown bat ( Eptesicus fuscus ) 49 . These results, together with ours show that the temporal context and spectrotemporal profile of the call-echo elements affect the response selectivity.…”

Enhanced representation of natural sound sequences in the ventral auditory midbrain

“…The echolocation sequence was recorded in a pendulum paradigm in which a bat was swung towards a reflective wall (Beetz et al 2016a ). Distress and echolocation sequences have been used in previous studies characterizing the bat auditory system (Beetz et al 2016a , 2017 ; Hechavarría et al 2016b ; Wohlgemuth and Moss 2016 ; Martin et al 2017 ; García-Rosales et al 2018 ; Macías et al 2018 ). To restrict the study to units that responded to the calls, we considered only those units that carried at least 1 bit/s of information (Kayser et al 2009 ) in response to at least one of the sequences studied (864 units out of 976).…”