The importance of complex behavior, or “Isn’t that awfully messy?”
We now have access to a variety of exquisitely precise tools for recording from, and even manipulating, populations of identified neurons in the intact behaving animal. The explosion in neurobiological tools has not, however, been matched by an increase in the quality and precision of behavioral analysis. At this point the bottleneck in understanding the nervous system is not tools, but behavioral assays that can take advantage of those tools.
The brain is not a tape recorder
It throws some things out and magnifies others. Animals live in complex and noisy environments. They extract useful information from these environments, cleaning up the noise (in general) to allow fantastically beautiful and adaptive behavior. This ability poses a problem for the neurobiologist—how do you study the representation of something if you don’t know what is being represented? One method, which has taught us a lot, is to make input stimuli or behaviors extremely simple—if there is only one useful feature in the stimulus, that must be what is being represented. However, the brain did not evolve to deal with simple stimuli; it evolved to deal with noise and mess. An alternative is to ask about the neural basis of behaviors the animal evolved to perform.
In our lab we embrace messiness
Our animals are socially housed (introducing dominance status, pregnancy, estrus state, age) in cages which mimic some of the features of wild mouse burrows. Animals don’t need massive repetition to make sensory discriminations, perform tasks, or navigate environments—so we think focusing on unpacking the neural code without averaging is important. Because of this we record from unrestrained, untrained mice during natural social behaviors.
We use several tools to tame the mess
One tool is theoretical—we work on vocalizations. Vocalizations are reasonably easy to record from a freely moving animal, and, importantly, vocalizations are an acoustic stimulus that mice are interested in attending to. When an animal is vocalizing, we know that at least some portions of the mouse’s nervous system are intent on vocal production—giving us a handle into representation on the motor side. Motor production rarely proceeds without feedback, so we also can look at the representation of the vocalization in the auditory system, as it is produced. In addition, a vocalization is a social signal, allowing us to record from the auditory systems of listening mice, with some belief that they are attending to the vocalizations.
Other tools are more technological—we have two active tracking projects (one video-based, one RFID-based) which allow us to make correlations between vocalizations and social interactions over long time scales. Video and RFID are complementary technologies—video provides high temporal and spatial resolution information, but identity is difficult, and data analysis to extract position information can be time consuming. RFID has low spatial and temporal resolution, but identity is perfect and data is recorded in an immediately biologically relevant way (mouse A and mouse B are in the same chamber).
motr (MOuse TRacker): motr is a fully automated tracking application that is capable of tracking multiple mice in a single enclosure over long periods of time (days) without confusing their identities. motr is an open-source (GPLv2), freely available program developed by Shay Ohayon, Pietro Perona (Caltech), Ofer Avni, Adam Taylor and Roian Egnor (Janelia Farm).
A quantitative description of animal social behaviour is informative for behavioural biologists and clinicians developing drugs to treat social disorders. Social interaction in a group of animals has been difficult to measure because behaviour develops over long periods of time and requires tedious manual scoring, which is subjective and often non-reproducible. Computer-vision systems with the ability to measure complex social behaviour automatically would have a transformative impact on biology. Here, we present a method for tracking group-housed mice individually as they freely interact over multiple days. Each mouse is bleach-marked with a unique fur pattern. The patterns are automatically learned by the tracking software and used to infer identities. Trajectories are analysed to measure behaviour as it develops over days, beyond the range of acute experiments. We demonstrate how our system may be used to study the development of place preferences, associations and social relationships by tracking four mice continuously for five days. Our system enables accurate and reproducible characterisation of wild-type mouse social behaviour and paves the way for high-throughput long-term observation of the effects of genetic, pharmacological and environmental manipulations.
Prior Publications (7)
Tracking silence: adjusting vocal production to avoid acoustic interference.Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 2007
R. S E. Egnor, J. Wickelgren, and M. D. Hauser Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 193:477-83 (2007)
Organisms that use vocal signals to communicate often modulate their vocalizations to avoid being masked by other sounds in the environment. Although some environmental noise is continuous, both biotic and abiotic noise can be intermittent, or even periodic. Interference from intermittent noise can be avoided if calls are timed to coincide with periods of silence, a capacity that is unambiguously present in insects, amphibians, birds, and humans. Surprisingly, we know virtually nothing about this fundamental capacity in nonhuman primates. Here we show that a New World monkey, the cotton-top tamarin (Saguinus oedipus), can restrict calls to periodic silent intervals in loud white noise. In addition, calls produced during these silent intervals were significantly louder than calls recorded in silent baseline sessions. Finally, average call duration dropped across sessions, indicating that experience with temporally patterned noise caused tamarins to compress their calls. Taken together, these results show that in the presence of a predictable, intermittent environmental noise, cotton-top tamarins are able to modify the duration, timing, and amplitude of their calls to avoid acoustic interference.
Auditory feedback is critical for the development and maintenance of speech in humans. In contrast, studies of nonhuman primate vocal production generally report that subjects show little reliance on auditory input. We examined the extent to which cotton-top tamarin (Saguinus oedipus) vocal production is sensitive to perturbation of auditory feedback by manipulating the predictability of presentation of a 1 s burst of white noise during the production of the species-specific contact call, the combination long call (CLC). We used three experimental conditions: the Begin condition, in which white noise was presented only during the first half of a recording session, the End condition, in which white noise was presented only in the last half, and the Random condition, in which each call had a 50% probability of receiving white noise playback throughout the recording session, making the auditory feedback unpredictable. In addition we recorded calls before and after the experimental series (Baseline condition) to determine whether any changes induced by modification of auditory feedback persisted. Results showed that playback of white noise during the production of the CLC produced changes in the temporal structure of the CLC: calls were shorter and had fewer pulses, indicating that modification of auditory feedback can interrupt vocal production. In addition, calls that received modified feedback were louder and had longer inter-pulse intervals than those that did not, consistent with an adaptive response to the masking effect of white noise playback. The magnitude of this compensatory effect and the interruption rate were both sensitive to whether the feedback modification occurred at the beginning or end of the experimental session: early feedback produced less interruption and more compensation. Finally, when auditory feedback modification was unpredictable, adaptive changes were observed in both calls that received modified feedback and those that received normal feedback, suggesting that tamarins can generate an expectation of noise playback and increase vocal amplitude in anticipation of masking.
The Lombard effect-an increase in vocalization amplitude in response to an increase in background noise-is observed in a wide variety of animals. We investigated this basic form of vocal control in the cotton-top tamarin (Saguinus oedipus) by measuring the amplitude of a contact call, the combination long call (CLC), while simultaneously varying the background noise level. All subjects showed a significant increase in call amplitude and syllable duration in response to an increase in background noise amplitude. Together with prior results, this study shows that tamarins have greater vocal control in the context of auditory feedback perturbation than previously suspected.
The importance of auditory feedback in the development of spoken language in humans is striking. Paradoxically, although auditory-feedback-dependent vocal plasticity has been shown in a variety of taxonomic groups, there is little evidence that our nearest relatives--non-human primates--require auditory feedback for the development of species-typical vocal signals. Because of the apparent lack of developmental plasticity in the vocal production system, neuroscientists have largely ignored the neural mechanisms of non-human primate vocal production and perception. Recently, the absence of evidence for vocal plasticity from developmental studies has been contrasted with evidence for vocal plasticity in adults. We argue that this new evidence makes non-human primate vocal behavior an attractive model system for neurobiological analysis.
Detection of large interaural delays and its implication for models of binaural interaction.Journal of the Association for Research in Otolaryngology : JARO 2002
K. Saberi, Y. Takahashi, R. Egnor, H. Farahbod, J. Mazer, and M. Konishi Journal of the Association for Research in Otolaryngology : JARO, 3:80-8 (2002)
The interaural time difference (ITD) is a major cue to sound localization along the horizontal plane. The maximum natural ITD occurs when a sound source is positioned opposite to one ear. We examined the ability of owls and humans to detect large ITDs in sounds presented through headphones. Stimuli consisted of either broad or narrow bands of Gaussian noise, 100 ms in duration. Using headphones allowed presentation of ITDs that are greater than the maximum natural ITD. Owls were able to discriminate a sound leading to the left ear from one leading to the right ear, for ITDs that are 5 times the maximum natural delay. Neural recordings from optic-tectum neurons, however, show that best ITDs are usually well within the natural range and are never as large as ITDs that are behaviorally discriminable. A model of binaural crosscorrelation with short delay lines is shown to explain behavioral detection of large ITDs. The model uses curved trajectories of a cross-correlation pattern as the basis for detection. These trajectories represent side peaks of neural ITD-tuning curves and successfully predict localization reversals by both owls and human subjects.
Effects of binaural decorrelation on neural and behavioral processing of interaural level differences in the barn owl (Tyto alba).Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 2001
S E. Egnor Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 187:589-95 (2001)
The effect of binaural decorrelation on the processing of interaural level difference cues in the barn owl (Tyto alba) was examined behaviorally and electrophysiologically. The electrophysiology experiment measured the effect of variations in binaural correlation on the first stage of interaural level difference encoding in the central nervous system. The responses of single neurons in the posterior part of the ventral nucleus of the lateral lemniscus were recorded to stimulation with binaurally correlated and binaurally uncorrelated noise. No significant differences in interaural level difference sensitivity were found between conditions. Neurons in the posterior part of the ventral nucleus of the lateral lemniscus encode the interaural level difference of binaurally correlated and binaurally uncorrelated noise with equal accuracy and precision. This nucleus therefore supplies higher auditory centers with an undegraded interaural level difference signal for sound stimuli that lack a coherent interaural time difference. The behavioral experiment measured auditory saccades in response to interaural level differences presented in binaurally correlated and binaurally uncorrelated noise. The precision and accuracy of sound localization based on interaural level difference was reduced but not eliminated for binaurally uncorrelated signals. The observation that barn owls continue to vary auditory saccades with the interaural level difference of binaurally uncorrelated stimuli suggests that neurons that drive head saccades can be activated by incomplete auditory spatial information.
Humans respond adaptively to uncertainty by escaping or seeking additional information. To foster a comparative study of uncertainty processes, we asked whether humans and a bottlenosed dolphin (Tursiops truncatus) would use similarly a psychophysical uncertain response. Human observers and the dolphin were given 2 primary discrimination responses and a way to escape chosen trials into easier ones. Humans escaped sparingly from the most difficult trials near threshold that left them demonstrably uncertain of the stimulus. The dolphin performed nearly identically. The behavior of both species is considered from the perspectives of signal detection theory and optimality theory, and its appropriate interpretation is discussed. Human and dolphin uncertain responses seem to be interesting cognitive analogs and may depend on cognitive or controlled decisional mechanisms. The capacity to monitor ongoing cognition, and use uncertainty appropriately, would be a valuable adaptation for animal minds. This recommends uncertainty processes as an important but neglected area for future comparative research.