An echolocating bat actively controls the spatial acoustic information that drives its behavior by directing its head and ears and by modulating the spectro-temporal structure of its outgoing sonar emissions. The superior colliculus may function in the coordination of these orienting components of the bat's echolocation system. To test this hypothesis, chemical and electrical microstimulation experiments were carried out in the superior colliculus of the echolocating bat, Eptesicus fuscus, a species that uses frequency modulated sonar signals. Microstimulation elicited pinna and head movements, similar to those reported in other vertebrate species, and the direction of the evoked behaviors corresponded to the site of stimulation, yielding a map of orienting movements in the superior colliculus. Microstimulation of the bat superior colliculus also elicited sonar vocalizations, a motor behavior specific to the bat's acoustic orientation by echolocation. Electrical stimulation of the adjacent periaqueductal gray, shown to be involved in vocal production in other mammalian species, elicited vocal signals resembling acoustic communication calls of E. fuscus. The control of vocal signals in the bat is an integral part of its acoustic orienting system, and our findings suggest that the superior colliculus supports diverse and species-relevant sensorimotor behaviors, including those used for echolocation.
Serotonin is a physiological signal that translates both internal and external information about behavioral context into changes in sensory processing through a diverse array of receptors. The details of this process, particularly how receptors interact to shape sensory encoding, are poorly understood. In the inferior colliculus, a midbrain auditory nucleus, serotonin (5-HT) 1A receptors have suppressive and 5-HT1B receptors have facilitatory effects on evoked responses of neurons. We explored how these two receptor classes interact by testing three hypotheses: that they 1) affect separate neuron populations, 2) affect different response properties, or 3) have different endogenous patterns of activation. The first two hypotheses were tested by iontophoretic application of 5-HT1A and 5-HT1B receptor agonists individually and together to neurons in vivo. 5-HT1A and 5-HT1B agonists affected overlapping populations of neurons. During coapplication, 5-HT1A and 5-HT1B agonists influenced spike rate and frequency bandwidth additively, with each moderating the effect of the other. In contrast, although both agonists individually influenced latencies and interspike intervals, the 5-HT1A agonist dominated these measurements during co-application. The third hypothesis was tested by applying antagonists of the 5-HT1A and 5-HT1B receptors. Blocking 5-HT1B receptors was complementary to activation of the receptor, but blocking 5-HT1A receptors was not, suggesting the endogenous activation of additional receptor types. These results suggest that cooperative interactions between 5-HT1A and 5-HT1B receptors shape auditory encoding in the IC, and that the effects of neuromodulators within sensory systems may depend nonlinearly on the specific profile of receptors that are activated.
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 (VTAD, Ϫ5.1 to Ϫ2.2 ms range, Ϫ3.6 Ϯ 0.7 ms mean lead time; ROTT, Ϫ3.0 to ϩ 0.4 ms range, Ϫ1.2 Ϯ 1.3 ms mean lead time), and this activity may play a role in marking the time of each sonar emission. A long lead bout in SC activity occurs earlier and spreads over a longer interval (VTAD, Ϫ40.6 to Ϫ8.4 ms range, Ϫ22.2 Ϯ 3.9 ms mean lead time; ROTT, Ϫ29.8 to Ϫ7.1 ms range, Ϫ17.5 Ϯ 9.1 ms mean lead time) 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.
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