Cortical neurons of bats respond best to echoes from nearest targets when listening to natural biosonar multi-echo streams

Abstract

Bats orientate in darkness by listening to echoes from their biosonar calls, a behaviour known as echolocation. Recent studies showed that cortical neurons respond in a highly selective manner when stimulated with natural echolocation sequences that contain echoes from single targets. However, it remains unknown how cortical neurons process echolocation sequences containing echo information from multiple objects. In the present study, we used echolocation sequences containing echoes from three, two or one object separated in the space depth as stimuli to study neuronal activity in the bat auditory cortex. Neuronal activity was recorded with multi-electrode arrays placed in the dorsal auditory cortex, where neurons tuned to target-distance are found. Our results show that target-distance encoding neurons are mostly selective to echoes coming from the closest object, and that the representation of echo information from distant objects is selectively suppressed. This suppression extends over a large part of the dorsal auditory cortex and may override possible parallel processing of multiple objects. The presented data suggest that global cortical suppression might establish a cortical “default mode” that allows selectively focusing on close obstacle even without active attention from the animals.

Echo interval and not echo intensity drives bat flight behavior in structured corridors

“…Neurophysiological studies in several bat species have measured single unit responses to broadcasts of natural echolocation sequences, which contained echoes from one or more objects (Bartenstein et al, 2014;Beetz et al, 2016Beetz et al, , 2017Greiter and Firzlaff, 2017;Macias et al, 2018;Sanderson and Simmons, 2000). For example, researchers presented the anesthetized FM bat Phyllostomus discolor with acoustic pulse-echo stimuli that simulated the bat's decreasing distance to one (Bartenstein et al, 2014) or two (Greiter and Firzlaff, 2017) objects, and characterized single-unit responses in the auditory cortex.…”

“…Single-unit responses to echolocation sequences containing up to three echoes have been characterized in the IC and auditory cortex of the anesthetized fruit bat Carollia perspicillata (Beetz et al, 2016(Beetz et al, , 2017. In these studies, acoustic stimuli contained call-echo segments of natural echolocation sequences that were recorded from a bat swinging on a pendulum, which passed by three objects.…”

Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat

“…(Bartenstein et al, 2014). In a related study, Beetz et al, 2016b show a higher probability of neural firing in cortical neurons of the bat species Carollia perspicillata to the first echo in a sequence, which leads them to hypothesize that global cortical inhibition contributes to the representation of the closest object, without active attention. It is possible that global cortical inhibition is an intrinsic feature, which enables an animal to represent the most salient (in the above case, closest) stimulus.…”

Bats dynamically change echolocation parameters in response to acoustic playback

“…Analysis of the call groups was conducted using custom-written scripts in Matlab 2014 (MathWorks, USA). Call groups were defined according to two criteria (Beetz et al, 2018;Kothari et al, 2014). An "island criterion" defined call groups that were isolated in time.…”

“…When swinging bats on the mass of a pendulum, they often emit echolocation calls (Beetz et al, 2016a;Henson et al, 1982;Macias et al, 2016). Thus, a pendulum paradigm allows to describe echolocation behavior under controlled conditions.…”