Vocal Premotor Activity in the Superior Colliculus

Hanging bats

    Chronic neural recordings were taken from the midbrain superior colliculus (SC) of echolocating bats while they were engaged in one of two distinct behavioral tasks: virtual target amplitude discrimination (VTAD) and real oscillating target tracking (ROTT). In the VTAD task, bats used a limited range of sonar call features to discriminate the amplitude category of echoes, whereas in the ROTT task, the bat produced dynamically modulated sonar calls to track a moving target. Newly developed methods for chronic recordings in unrestrained, behaving bats reveal two consistent bouts of SC neural activity preceding the onset of sonar vocalizations in both tasks. A short lead bout occurs tightly coupled to vocal onset, and this activity may play a role in marking the time of each sonar emission. Along lead bout in SC activity occurs earlier and spreads over a longer interval when compared with short lead events. In the goal-directed ROTT task, the timing of long lead event times vary with the bat’s sonar call duration. This finding, along with behavioral studies demonstrating that bats adjust sonar call duration as they track targets at changing distance, suggests the bat SC contributes to range-dependent adjustments of sonar call duration.

    sonar vocal
    Sonar vocal behavior, audiovocal neuronal circuitry, dorsal SC position, and experimental subject. A, Time waveform and selected spectrograms of a sequence of sonar vocalizations produced by a flying bat attacking a stationary insect target. Typical of an insect pursuit sequence, there are dynamic changes in the sonar pulse intervals as bats approach and capture a target (top). The representative spectrograms demonstrate the change in bandwidth, call duration, and sweep rate during insect capture (bottom). Asterisks are positioned below calls for which spectrograms are shown. B, Network of input– output pathways that connect the SC with the sonar vocal production circuitry. Lemniscal (black arrow, top) and paralemniscal (gray arrow, at side) auditory inputs are integrated in the SC, which in turn projects to the laryngeal motor neurons indirectly via a tecto-tegementobulbar pathway. C, Top view drawing of the bat brain showing the dorsomedial position and relative size of the superior colliculus compared with adjacent structures. CBR, Cerebrum; CBL, cerebellum. Scale bar, 5 mm. D, Photograph of a 15 g bat with chronic implant before recording session. The small interface board mates with a removable amplifier head-stage board.
    sonar vocal
    Premotor neuronal activity recorded in the SC during a single oscillating target trial. A, Raster and perimotor time histogram show a pattern of premotor activity similar to that observed in virtual target amplitude discrimination recordings. LLEs and SLEs precede sonar vocalizations with a reduction toward baseline activity rates between the two event groups. Data are aligned to sonar call onset (lead time of t 0 ms). LLEs in the raster show a tendency toward shorter lead times during the trial and correspond to timeswhenthe target is approaching the bat.B, PI (gray, filled), start (black, filled), and end (black, open) frequency, call duration (black, open), and target distance (black, filled) of sonar vocalizations produced during trial shown inA. The oscillating target approaches and recedes from the bat twice in this trial. Each sonar call parameter is modulated as a function of the target distance. Sonar call duration and pulse interval are clearly decreased whenever the target approaches. C, Linear regression using the per call mean LLE time ( LLE TIME) as the single predictor of sonar call duration for all sonar calls in one recording session (n 738 calls). The data show an increase in LLE TIME for increasing sonar call durations (r 0.73). D, Reduction in the correlation between sonar call duration and LLE TIME when LLE TIME is not associated with the call it precedes. Each panel shows the sonar call duration versus the LLE TIME using the data from C. Except for the top left, the other panels show the data with LLE TIME associated with the sonar call duration one, three, and five calls ahead in the vocal sequence. r values are regression coefficients.