Optimal Local Estimates of Visual Motion in a Natural Environment.

Many organisms use visual signals to estimate motion, and these estimates typically are biased. Here, we ask whether these biases may reflect physical rather than biological limitations. Using a camera-gyroscope system, we sample the joint distribution of images and rotational motions in a natural environment, and from this distribution we construct the optimal estimator of velocity based on local image intensities. Over most of the natural dynamic range, this estimator exhibits the biases observed in neural and behavioral responses. Thus, imputed errors in sensory processing may represent an optimal response to the physical signals sampled from the environment.

Encoding of yaw in the presence of distractor motion: studies in a fly motion sensitive neuron.

Motion estimation is crucial for aerial animals such as the fly, which perform fast and complex maneuvers while flying through a 3-D environment. Motion-sensitive neurons in the lobula plate, a part of the visual brain, of the fly have been studied extensively for their specialized role in motion encoding. However, the visual stimuli used in such studies are typically highly simplified, often move in restricted ways, and do not represent the complexities of optic flow generated during actual flight. Here, we use combined rotations about different axes to study how H1, a wide-field motion-sensitive neuron, encodes preferred yaw motion in the presence of stimuli not aligned with its preferred direction. Our approach is an extension of "white noise" methods, providing a framework that is readily adaptable to quantitative studies into the coding of mixed dynamic stimuli in other systems. We find that the presence of a roll or pitch ("distractor") stimulus reduces information transmitted by H1 about yaw, with the amount of this reduction depending on the variance of the distractor. Spike generation is influenced by features of both yaw and the distractor, where the degree of influence is determined by their relative strengths. Certain distractor features may induce bidirectional responses, which are indicative of an imbalance between global excitation and inhibition resulting from complex optic flow. Further, the response is shaped by the dynamics of the combined stimulus. Our results provide intuition for plausible strategies involved in efficient coding of preferred motion from complex stimuli having multiple motion components.

5-HT1A and 5-HT1B receptors differentially modulate rate and timing of auditory responses in the mouse inferior colliculus.

Serotonin (5-hydroxytryptamine; 5-HT) 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, 5-HT1A 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 (i) affect separate neuron populations; (ii) affect different response properties; or (iii) 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 co-application, 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 inferior colliculus, and that the effects of neuromodulators within sensory systems may depend nonlinearly on the specific profile of receptors that are activated.

Vocal premotor activity in the superior colliculus.

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, -5.1 to -2.2 ms range, -3.6 +/- 0.7 ms mean lead time; ROTT, -3.0 to + 0.4 ms range, -1.2 +/- 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, -40.6 to -8.4 ms range, -22.2 +/- 3.9 ms mean lead time; ROTT, -29.8 to -7.1 ms range, -17.5 +/- 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.

Neurobiology of echolocation in bats.

Echolocating bats (sub-order: Microchiroptera) form a highly successful group of animals, comprising approximately 700 species and an estimated 25% of living mammals. Many echolocating bats are nocturnal predators that have evolved a biological sonar system to orient and forage in three-dimensional space. Acoustic signal processing and vocal-motor control are tightly coupled, and successful echolocation depends on the coordination between auditory and motor systems. Indeed, echolocation involves adaptive changes in vocal production patterns, which, in turn, constrain the acoustic information arriving at the bat's ears and the time-scales over which neural computations take place.

Orienting responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus.

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.