Role of the midbrain superior colliculus in audiomotor integration

Brittney Boublil

Echolocating bats have evolved specializations to navigate and forage in the dark, using biological sonar. Echolocating bats produce high frequency sounds and process information in the returning echoes to localize objects in space and guide orienting behaviors.1,2,3 Importantly, bats adapt the features of the sonar signals they produce in response to spatial information they extract from returning echoes.4 The big brown bat (Eptesicus fuscus), the subject of my research, increases the rate of vocal production and decreases the duration of each emitted call as it approaches and prepares to intercept prey.4,5 The success of bat sonar imaging depends critically on this audiomotor feedback system.

Past research on the mechanisms of bat echolocation has focused on sound processing along the auditory pathway, typically with simulated calls and echoes, with few studies of the audiomotor feedback system, which is fundamental to biological sonar imaging. My research aims to fill this research gap by conducting studies of the superior colliculus (SC), a midbrain structure implicated in sensorimotor integration and goal-directed orienting movements of the eyes, head and ears. 6 In mammals, the superficial layers of the SC receive direct input from the retina. The intermediate and deep layers receive inputs from visual, auditory, somatosensory, and motor pathways. Traditionally, the SC has been studied with respect to its role in visuomotor integration, and previous SC inactivation studies in non-human primates have shown that the SC plays an important functional role in visual target tracking and selection.7 Specifically, researchers discovered that inactivation of the SC in Rhesus monkeys disrupted goal-directed eye movements.7 Echolocating bats, unlike other mammals, lack the ability to move their eyes and do not rely heavily on visual input to orient themselves to objects in their surroundings.1,8 Instead, they rely on sound to localize objects in their environment and navigate.

Prior research on the functional role of the SC in the big brown bat demonstrated that activation of local pools of neurons through microstimulation elicits movements of the head and ears. This work showed that the direction of movement is dependent on the location of microstimulation in the SC, revealing a topographic motor map of head and ear movements.9 Additionally, microstimulation in the bat SC elicits sonar signal production, which is an essential component of its acoustic orienting behavior. Early behavioral studies showed that SC lesions do not affect bat performance in an obstacle avoidance task10; however, the obstacle avoidance test did not tap into the animal’s goal-directed orienting behavior. Instead, preliminary studies provide evidence that the bat SC plays a role in coordinating goal-directed orienting behaviors.11,12 My research will test the hypothesis that the SC orchestrates the temporal coordination between echo processing and adaptive motor behaviors to enable precise target tracking and interception.

Experiment 1:

I will conduct studies to investigate the effect of chemical inactivation of the SC on the temporal coordination of head and ear movements, vocal production and echo processing in bats tracking sonar targets. Big brown bats will be trained to rest on a platform and track a moving target, a tethered mealworm, Tenebrio molitor. The tethered insect will be connected to a set of four pulleys and a rotary motor, which will allow for control over the direction, velocity, and acceleration of the target (Fig. 1). Once bats reliably track the moving target from 2.5 meters from their resting position on the platform, I will chronically implant metal cannulas bilaterally into the SC. Following a four to five-day recovery period, bats will enter the testing phase of the experiment.

Fig. 1. Behavioral setup for platform target-tracking experiment.
Adapted from Wohlgemuth et al. (2016).

In the testing phase, bats will begin in a baseline session, where they will track a moving tethered mealworm. This will then be followed by an inactivation session. Here, I will temporarily inactivate the SC using a 20 nanoliter intracranial infusion of fluorescent muscimol. Muscimol is a GABAA (γ-aminobutyric acid) agonist that acts by binding to GABAA receptors at the site of injection and depresses neural activity in restricted regions of the brain. The bats will perform a second baseline session 24 hours after the inactivation session for comparison. In control conditions, I will infuse 20 nanoliters of artificial cerebral spinal fluid (aCSF) in the SC. The bat’s echolocation behavior, head position, and ear movements will be recorded as it tracks the moving target.

Experiment 2:
Fig. 2. Behavioral setup for free-flight experiment.

I will study the effect of chemical inactivation of the SC on goal-oriented behaviors in free-flying bats. I will train big brown bats to capture a tethered mealworm in the laboratory flight room (Fig. 2). Once bats reach a criterion of 70% insect capture success, I will chronically implant metal cannulas bilaterally into the SC. Once the batsí post-operative performance reaches pre-training performance levels, they will enter the experimental phase. Bats will be tested using the same SC chemical inactivation protocol outlined in Experiment 1. In this experiment, I will study bat coordinated flight and echolocation behaviors by taking synchronized, high-speed audio and video recordings. Audio recordings will be used to quantify the directional aim, rate/interval, and duration of echolocation calls. Similar to the platform target-tracking experiment, I hypothesize that the coordination between the bats’ flight and echolocation behaviors will be disrupted by bilateral inactivation of the SC, which will, in turn, interfere with bats’ insect capture performance.

References

1. Griffin, D.R. (1958). Listening in the dark. New Haven: Yale UP.

2. Moss, C. F., & Sinha, S. R. (2003). Neurobiology of echolocation. CONB,13(6), 751-758.

3. Ulanovsky, N., & Moss, C. F. (2008). What the bat's voice tells the bat's brain, PNAS, 105(25), 8491-8498.

4. Surlykke, A., & Moss, C. F. (2000). Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory, JASA, 108(5), 2419- 2429.

5. Simmons, J. A. (1979). Perception of echo phase information in bat sonar, Science, 204(4399), 1336- 1338.

6. Gandhi, N. J., & Katnani, H. A. (2011). Motor functions of the superior colliculus. Ann. Rev. Neurosci., 34, 205.

7. McPeek, R. M., & Keller, E. L. (2004). Deficits in saccade target selection after inactivation of superior colliculus, Nature Neurosci., 7(7), 757-763.

8. Walls, G. L. (1942). The vertebrate eye and its adaptive radiation. Bloomfield Hills, Mich., Cranbrook Institute of Science.

9. Valentine, D. E., Sinha, S. R., & Moss, C. F. (2002). Orienting responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus. JCPA, 188(2), 89-108.

10. Wenstrup, J.J., & Suthers, R.A. (1981). Do lesions of the superior colliculus affect acoustic orientation in echolocating bats?, Physiol. & Behav. 27(5), 835-839.

11. Valentine, D.E. & Moss, C.F. (1998). Sensorimotor integration in bat sonar. In T.H. Kunz and P.A. Racey (Editors) Bats: Phylogeny, Morphology, Echolocation and Conservation Biology. Smithsonian Institution Press, Washington, D.C., 1998, 220-230.

12. Wohlgemuth, M.J., Kothari, N.B. & Moss, C.F. Midbrain Functional Organization and Dynamic Activity in the Superior Colliculus of the Echolocating Bat, Eptesicus fuscus, J. Neurosci, in press.

13. Covey, E., Hall, W.C., & Kobler, J.B. (1987). Subcortical connections of the superior colliculus in the mustache bat, Pteronotus parnellii. J. Comp. Neurol., 263(2), 179-197.

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