Melville J. Wohlgemuth

Central Contributions to Acoustic Variation in Birdsong

Birdsong is a learned behavior remarkable for its high degree of stereotypy. Nevertheless, adult birds display substantial rendition-by-rendition variation in the structure of individual song elements or “syllables.” Previous work suggests that some of this variation is actively generated by the avian basal ganglia circuitry for purposes of motor exploration. However, it is unknown whether and how natural variations in premotor activity drive variations in syllable structure. Here, we recorded from the premotor nucleus robust nucleus of the arcopallium (RA) in Bengalese finches and measured whether neural activity covaried with syllable structure across multiple renditions of individual syllables. We found that variations in premotor activity were significantly correlated with variations in the acoustic features (pitch, amplitude, and spectral entropy) of syllables in approximately a quarter of all cases. In these cases, individual neural recordings predicted 8.5 ± 0.3% (mean ± SE) of the behavioral variation, and in some cases accounted for 25% or more of trial-by-trial variations in acoustic output. The prevalence and strength of neuron–behavior correlations indicate that each acoustic feature is controlled by a large ensemble of neurons that vary their activity in a coordinated manner. Additionally, we found that correlations with pitch (but not other features) were predominantly positive in sign, supporting a model of pitch production based on the anatomy and physiology of the vocal motor apparatus. Collectively, our results indicate that trial-by-trial variations in spectral structure are indeed under central neural control at the level of RA, consistent with the idea that such variation reflects motor exploration.

Linked control of syllable sequence and phonology in birdsong

The control of sequenced behaviors, including human speech, requires that the brain coordinate the production of discrete motor elements with their concatenation into complex patterns. In birdsong, another sequential vocal behavior, the acoustic structure (phonology) of individual song elements, or “syllables,” must be coordinated with the sequencing of syllables into a song. However, it is unknown whether syllable phonology is independent of the sequence in which a syllable is produced. We quantified interactions between phonology and sequence in Bengalese finch song by examining both convergent syllables, which can be preceded by at least two different syllables and divergent syllables, which can be followed by at least two different syllables. Phonology differed significantly based on the identity of the preceding syllable for 97% of convergent syllables and differed significantly with the identity of the upcoming syllable for 92% of divergent syllables. Furthermore, sequence-dependent phonological differences extended at least two syllables away from the convergent or divergent syllable. To determine whether these phenomena reflect differences in central control, we analyzed premotor neural activity in the robust nucleus of the arcopallium (RA). Activity associated with a syllable varied significantly depending on the sequence in which the syllable was produced, suggesting that sequence-dependent variations in premotor activity contribute to sequence-dependent differences in phonology. Moreover, these data indicate that RA activity could contribute to the sequencing of syllables. Together, these results suggest that, rather than being controlled independently, the sequence and phonology of birdsong are intimately related, as is the case for human speech.

Timing matters: sonar call groups facilitate target localization in bats

To successfully negotiate a cluttered environment, an echolocating bat must control the timing of motor behaviors in response to dynamic sensory information. Here we detail the big brown bats adaptive temporal control over sonar call production for tracking prey, moving predictably or unpredictably, under different experimental conditions. We studied the adaptive control of vocal-motor behaviors in free-flying big brown bats, Eptesicus fuscus, as they captured tethered and free-flying insects, in open and cluttered environments. We also studied adaptive sonar behavior in bats trained to track moving targets from a resting position. In each of these experiments, bats adjusted the features of their calls to separate target and clutter. Under many task conditions, flying bats produced prominent sonar sound groups identified as clusters of echolocation pulses with relatively stable intervals, surrounded by longer pulse intervals. In experiments where bats tracked approaching targets from a resting position, bats also produced sonar sound groups, and the prevalence of these sonar sound groups increased when motion of the target was unpredictable. We hypothesize that sonar sound groups produced during flight, and the sonar call doublets produced by a bat tracking a target from a resting position, help the animal resolve dynamic target location and represent the echo scene in greater detail. Collectively, our data reveal adaptive temporal control over sonar call production that allows the bat to negotiate a complex and dynamic environment.

Three-dimensional auditory localization in the echolocating bat.

Echolocating bats exhibit accurate three-dimensional (3D) auditory localization to avoid obstacles and intercept prey. The bat achieves high spatial resolution through a biological sonar system. Key features of the bats sonar system are (1) high frequency, directional echolocation signals; (2) high frequency hearing; (3) mobile ears; and (4) measurement of distance from the time delay between sonar emission and echo reception. The bats sonar receiver is a standard mammalian auditory system that computes azimuth from inter-aural differences and elevation from spectral filtering by the ear [1-3]. Target range is computed from echo arrival time [4,5], and the bat auditory system contains neurons that show echo delay-tuned responses to pulse-echo pairs [6]. Ultimately, information about sound source azimuth, elevation and range converge to create a unified representation of 3D space.

Action Enhances Acoustic Cues for 3-D Target Localization by Echolocating Bats.

Under natural conditions, animals encounter a barrage of sensory information from which they must select and interpret biologically relevant signals. Active sensing can facilitate this process by engaging motor systems in the sampling of sensory information. The echolocating bat serves as an excellent model to investigate the coupling between action and sensing because it adaptively controls both the acoustic signals used to probe the environment and movements to receive echoes at the auditory periphery. We report here that the echolocating bat controls the features of its sonar vocalizations in tandem with the positioning of the outer ears to maximize acoustic cues for target detection and localization. The bat’s adaptive control of sonar vocalizations and ear positioning occurs on a millisecond timescale to capture spatial information from arriving echoes, as well as on a longer timescale to track target movement. Our results demonstrate that purposeful control over sonar sound production and reception can serve to improve acoustic cues for localization tasks. This finding also highlights the general importance of movement to sensory processing across animal species. Finally, our discoveries point to important parallels between spatial perception by echolocation and vision.

Midbrain auditory selectivity to natural sounds

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. 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.

Functional organization and dynamic activity in the superior colliculus of the echolocating bat, Eptesicus fuscus

Sensory-guided behaviors require the transformation of sensory information into task-specific motor commands. Prior research on sensorimotor integration has emphasized visuomotor processes in the context of simplified orienting movements in controlled laboratory tasks rather than an animals more complete, natural behavioral repertoire. Here, we conducted a series of neural recording experiments in the midbrain superior colliculus (SC) of echolocating bats engaged in a sonar target-tracking task that invoked dynamic active sensing behaviors. We hypothesized that SC activity in freely behaving animals would reveal dynamic shifts in neural firing patterns within and across sensory, sensorimotor, and premotor layers. We recorded neural activity in the SC of freely echolocating bats (three females and one male) and replicated the general trends reported in other species with sensory responses in the dorsal divisions and premotor activity in ventral divisions of the SC. However, within this coarse functional organization, we discovered that sensory and motor neurons are comingled within layers throughout the volume of the bat SC. In addition, as the bat increased pulse rate adaptively to increase resolution of the target location with closing distance, the activity of sensory and vocal premotor neurons changed such that auditory response times decreased, and vocal premotor lead times shortened. This finding demonstrates that SC activity can be modified dynamically in concert with adaptive behaviors and suggests that an integrated functional organization within SC laminae supports rapid and local integration of sensory and motor signals for natural, adaptive behaviors. SIGNIFICANCE STATEMENT Natural sensory-guided behaviors involve the rapid integration of information from the environment to direct flexible motor actions. The vast majority of research on sensorimotor integration has used artificial stimuli and simplified behaviors, leaving open questions about nervous system function in the context of natural tasks. Our work investigated mechanisms of dynamic sensorimotor feedback control by analyzing patterns of neural activity in the midbrain superior colliculus (SC) of an echolocating bat tracking and intercepting moving prey. Recordings revealed that sensory and motor neurons comingle within laminae of the SC to support rapid sensorimotor integration. Further, we discovered that neural activity in the bat SC changes with dynamic adaptations in the animals echolocation behavior.

Midbrain neurons of the free-flying echolocating bat represent three-dimensional space

Spatial navigation by echolocation in bats is an active and adaptive system: Its success depends upon tight coupling between motor commands for sonar signal production and neural processing that supports spatial perception and attention to objects in the 3D environment. The midbrain superior colliculus (SC) has been implicated in sensorimotor transformations to support adaptive behaviors in the echolocating bat, but the response properties of SC neurons have yet to be studied in free-flying animals engaged in natural spatial navigation behaviors. Using RF telemetry, in combination with a model that computes the direction and arrival time of echoes received at the bat’s ears, we have successfully characterized the auditory response profiles of single neurons in the SC of the free-flying big brown bat. Neural data, acquired across intermediate and deep layers of the bat SC, were sorted off-line from multichannel silicon array recordings. Spikes evoked by echo returns were analyzed and used to construct 3D s...

Adaptive sonar call timing supports target tracking in echolocating bats

ABSTRACT Echolocating bats dynamically adapt the features of their sonar calls as they approach obstacles and track targets. As insectivorous bats forage, they increase sonar call rate with decreasing prey distance, and often embedded in bat insect approach sequences are clusters of sonar sounds, termed sonar sound groups (SSGs). The bats production of SSGs has been observed in both field and laboratory conditions, and is hypothesized to sharpen spatiotemporal sonar resolution. When insectivorous bats hunt, they may encounter erratically moving prey, which increases the demands on the bats sonar imaging system. Here, we studied the bats adaptive vocal behavior in an experimentally controlled insect-tracking task, allowing us to manipulate the predictability of target trajectories and measure the prevalence of SSGs. With this system, we trained bats to remain stationary on a platform and track a moving prey item, whose trajectory was programmed either to approach the bat, or to move back and forth, before arriving at the bat. We manipulated target motion predictability by varying the order in which different target trajectories were presented to the bats. During all trials, we recorded the bats sonar calls and later analysed the incidence of SSG production during the different target tracking conditions. Our results demonstrate that bats increase the production of SSGs when target unpredictability increases, and decrease the production of SSGs when target motion predictability increases. Furthermore, bats produce the same number of sonar vocalizations irrespective of the target motion predictability, indicating that the animals temporal clustering of sonar call sequences to produce SSGs is purposeful, and therefore involves sensorimotor planning. Summary: Echolocating bats increase production of temporally clustered sonar calls when tracking targets with unpredictable trajectories, providing evidence that bats control sonar signal timing for increased spatiotemporal resolution and sensorimotor planning.

3D Hippocampal Place Field Dynamics in Free-Flying Echolocating Bats

A large body of laboratory research has investigated the process by which environmental cues are acquired and used for spatial navigation in rodents; however, the key to differentiating between species specializations and general principles lies in comparative research. Rodent research has focused on a class of neurons in the hippocampus implicated in the representation of allocentric space – termed place cells – and the process by which these representations form. One class of models of hippocampal place field formation depends on continuous theta, a low frequency brain oscillation that is prevalent in crawling rodents. Comparative studies of hippocampal activity in echolocating bats have reported many findings that parallel the rodent literature, but also describe noteworthy species differences, especially with respect to theta rhythm. Here, we first discuss studies of the bat hippocampal formation and point to gaps in our knowledge, which motivate our new lines of inquiry. We present data from the free-flying laryngeal echolocating big brown bat, which shows 3-D place cells without continuous theta, similar to reports from the lingual echolocating Egyptian fruit bat. We also report findings, which demonstrate that the animal’s control over echolocation call rate (sensory sampling) influences place field tuning. These results motivate future comparative research on hippocampal function in the context of natural sensory-guided behaviors.