Neural Mechamisms for Sensorimotor Integration:

Role of the Superior Colliculus

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Our aim in this research is to understand general principles guiding the functional role of the vertebrate midbrain in sensorimotor behavior. Adaptive behaviors to dynamic acoustic information require a sensorimotor interface, where spatial information from echoes is used to guide appropriate motor responses. The midbrain superior colliculus (SC) is thought to play a role in transforming polymodal sensory information into signals relayed to premotor and motor structures in the brainstem that control appropriate orienting responses, such as visually-guided eye movements.

By analogy,the SC of the echolocating bat may play a role in the orienting behaviors that support echolocation, and we are studying the functional organization of the bat SC and its possible role in the sensorimotor integration essential to biosonar. In particular, this line of research explores the role of the SC in an adaptive system that coordinates the bat's vocal-motor control over the acoustic features of target echoes.

A. Dorsal view of the brain of
Eptesicus Fuscus

B. Cross-section showing laminar structure of superior colliculus (SC)

PAG=Periaqueductal Grey
SC=Superior Colliculus
MGB=Medial geniculate body
IC=Inferior Colliculus
CBL=Cerebellum

Extracellular Recording

We have discovered a population of auditory neurons in the intermediate and deep layers of the bat SC that shows facilitated or delay-tuned responses to pairs of sounds, simulating sonar emissions and echoes, and delay-tuned responses are believed to be related to the encoding of target range. Activity in this population of neurons may be important to the bat's echolocation behavior, since changes in its sonar sounds are closely tied to changes in target range. Our work in this area now focuses on detailed mapping of echo delay-tuned neurons in the SC of the bat, with the aim of delineating the functional organization of neurons that may encode distance information to guide appropriate motor responses. We are also beginning experiments that examine spatial response profiles of auditory neurons in behaving animals.

Speaker hoop that allows sound delivery from different azimuths and elevations

Microstimulation

Our studies of the bat SC have also included microstimulation experiments, and we have elicited pinna and head movements via electrical pulse trains in the bat midbrain. In addition, we have found that SC microstimulation can produce sonar vocalizations coupled to head movements, a result not observed in other mammals. As vocal behavior in the bat is an integral part of its acoustic orientation, this observation fits with the general notion that the SC is involved in coordinating species-appropriate orienting behaviors. We are now analyzing the motor behaviors elicited by stimulation at different sites within the SC, with the goal of understanding the underlying motor coordinate system in this neural structure.

Art work by Mary Ellen Morris

A. Motor map of pinna
movements
in the bat superior colliculus

B. Microstimulation of the
bat superior elicits
head movements
that depend on
the site of stimulation.

From Valentine and Moss,
1998.

Sonar sounds are recorded on a high speed reel-to-reel recorder or digital acquisition system and analyzed offline.

Schematic of setup in microstimulation experiments:

M1 and M2 are microphones placed to recording electrically or chemically elicited vocalizations.

Video camera records pinna and head movements

Vocalizations elicited by midbrain microstimulation
A. Monopolar SC Stimulation B. Bipolar SC Stimulation C. PAG Stimulation D. Vocalization from a free-flying bat

Microstimulation of
the bat superior colliculus
elicits pinna
& head movements
and sonar vacalizations
at different
response latencies

Echo delay tuned neuron

A population of
neurons
in the bat SC show
selective responses to
simulated pulse-echo pairs

A population of
auditory neurons
in the bat
superior colliculus
show spatial selectivity
to azimuth, elevation
and range(echo delay)

Bursts of neural activity
in the bat SC coincide with
the production of
sonar vocalizations

Echolocating bats are nocturnal predators that have evolved a biological sonar system. They scan and probe their complex environment using rapid sequences of constant frequency (CF) and/or frequency modulated (FM) ultrasonic vocalizations. One neural structure involved in orienting is the mammalian superior colliculus. To date we have shown that the midbrain superior colliculus of the echolocating bat has specializations that support the orienting of acoustic gaze. Three lines of evidence currently provide support for its role in influencing sonar vocalizations.

1. Populations of auditory neurons that show 2-D (directional: azimuth and elevation) and 3-D (direction and range) spatial tuning of their auditory receptive fields (Valentine and Moss, 1997).

2. Chemical and electrical microstimulation of the superior colliculus elicits species-specific sonar vocalizations, as well as head and pinna movements (Valentine et al., 2002) (Schuller and Radtke-Schuller, 1990).

3. Tracer injections into the superior colliculus show connections with brainstem motor pathways involved in the control of orienting behaviors (Sinha et al., 2000).

Recent experiments conducted in the lab attempt to elucidate the functional role of the superior colliculus in sonar vocal production. To this end chronic neural recording methods have been developed to record neural activity from freely behaving, unrestrained bats, engaged in behavioral tasks.

We have demonstrated bursts of neural activity preceding and correlated with sonar vocalizations. These bursts are correlated with the duration and pulse interval of sonar cries the bat produces. Duration is a parameter tightly controlled by bats as they approach insect targets, and the pattern of pre-motor activity observed in the superior colliculus may reflect and adjustment of the distance to which a bat is attending.

Reference List

1. Schuller G, Radtke-Schuller S (1990) Neural control of vocalization in bats: mapping of brainstem areas with electrical microstimulation eliciting species-specific echolocation calls in the rufous horseshoe bat. Exp Brain Res 79: 192-206.

2. Valentine DE, Moss CF (1997) Spatially selective auditory responses in the superior colliculus of the echolocating bat. J Neurosci 17: 1720-1733.

3. Valentine DE, Sinha SR, Moss CF (2002) Orienting responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188: 89-108.

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