Emergent tuning for learned vocalizations in auditory cortex.

Vocal learners use early social experience to develop auditory skills specialized for communication. However, it is unknown where in the auditory pathway neural responses become selective for vocalizations or how the underlying encoding mechanisms change with experience. We used a vocal tutoring manipulation in two species of songbird to reveal that tuning for conspecific song arises within the primary auditory cortical circuit. Neurons in the deep region of primary auditory cortex responded more to conspecific songs than to other species' songs and more to species-typical spectrotemporal modulations, but neurons in the intermediate (thalamorecipient) region did not. Moreover, birds that learned song from another species exhibited parallel shifts in selectivity and tuning toward the tutor species' songs in the deep but not the intermediate region. Our results locate a region in the auditory processing hierarchy where an experience-dependent coding mechanism aligns auditory responses with the output of a learned vocal motor behavior.

Concerted and mosaic evolution of functional modules in songbird brains.

Vertebrate brains differ in overall size, composition and functional capacities, but the evolutionary processes linking these traits are unclear. Two leading models offer opposing views: the concerted model ascribes major dimensions of covariation in brain structures to developmental events, whereas the mosaic model relates divergent structures to functional capabilities. The models are often cast as incompatible, but they must be unified to explain how adaptive changes in brain structure arise from pre-existing architectures and developmental mechanisms. Here we show that variation in the sizes of discrete neural systems in songbirds, a species-rich group exhibiting diverse behavioural and ecological specializations, supports major elements of both models. In accordance with the concerted model, most variation in nucleus volumes is shared across functional domains and allometry is related to developmental sequence. Per the mosaic model, residual variation in nucleus volumes is correlated within functional systems and predicts specific behavioural capabilities. These comparisons indicate that oscine brains evolved primarily as a coordinated whole but also experienced significant, independent modifications to dedicated systems from specific selection pressures. Finally, patterns of covariation between species and brain areas hint at underlying developmental mechanisms.

Motor pathway convergence predicts syllable repertoire size in oscine birds.

Behavioral specializations are frequently associated with expansions of the brain regions controlling them. This principle of proper mass spans sensory, motor, and cognitive abilities and has been observed in a wide variety of vertebrate species. Yet, it is unknown if this concept extrapolates to entire neural pathways or how selection on a behavioral capacity might otherwise shape circuit structure. We investigate these questions by comparing the songs and neuroanatomy of 49 species from 17 families of songbirds, which vary immensely in the number of unique song components they produce and possess a conserved neural network dedicated to this behavior. We find that syllable repertoire size is strongly related to the degree of song motor pathway convergence. Repertoire size is more accurately predicted by the number of neurons in higher motor areas relative to that in their downstream targets than by the overall number of neurons in the song motor pathway. Additionally, the convergence values along serial premotor and primary motor projections account for distinct portions of the behavioral variation. These findings suggest that selection on song has independently shaped different components of this hierarchical pathway, and they elucidate how changes in pathway structure could have underlain elaborations of this learned motor behavior.

Coevolution in communication senders and receivers: vocal behavior and auditory processing in multiple songbird species.

Communication is a strong selective pressure on brain evolution because the exchange of information between individuals is crucial for fitness-related behaviors, such as mating. Given the importance of communication, the brains of signal senders and receivers are likely to be functionally coordinated. We study vocal behavior and auditory processing in multiple species of estrildid finches with the goal of understanding how species identity and early experience interact to shape the neural systems that subserve communication. Male finches learn to produce species-specific songs, and both sexes learn to recognize songs. Our studies indicate that closely related species exhibit different auditory coding properties in the midbrain and forebrain and that early life experience of vocalizations contributes to these differences. Moreover, birds that naturally sing tonal songs can learn broadband songs from heterospecific tutors, providing an opportunity to examine the interplay between species identity and early experience in the development of vocal behavior and auditory tuning.

Can measures of sound localization acuity be related to the precision of absolute location estimates?

Studies of sound localization use relative or absolute psychoacoustic paradigms. Relative tasks assess acuity by determining the smallest angle separating two sources that subjects can discriminate, the minimum audible angle (MAA), whereas absolute tasks measure subjects' abilities to indicate sound location. It is unclear whether or how measures from the two tasks are related, though the belief that the MAA is specifically related to the precision of absolute localization is common. The present study aimed to investigate the basis of this relationship by comparing the precision of absolute location estimates with a measure of spatial acuity computed from the same data. Three cats were trained to indicate apparent sound source locations that varied in azimuth and elevation via orienting gaze shifts (combined eye and head movements). The precision of these absolute responses, as measured by their standard deviation, was compared with acuity thresholds derived from receiver operating characteristic (ROC) analyses of the cumulative distributions. Surprisingly, the acuity measures were occasionally very poor indicators of absolute localization precision. Incongruent results were attributed to errors in mean accuracy, which are disregarded in analyses of traditional relative tasks. Discussion focuses on the potential for internal biases to affect measures of localization acuity.

Sound-localization performance in the cat: the effect of restraining the head.

In oculomotor research, there are two common methods by which the apparent location of visual and/or auditory targets are measured, saccadic eye movements with the head restrained and gaze shifts (combined saccades and head movements) with the head unrestrained. Because cats have a small oculomotor range (approximately +/-25 degrees), head movements are necessary when orienting to targets at the extremes of or outside this range. Here we tested the hypothesis that the accuracy of localizing auditory and visual targets using more ethologically natural head-unrestrained gaze shifts would be superior to head-restrained eye saccades. The effect of stimulus duration on localization accuracy was also investigated. Three cats were trained using operant conditioning with their heads initially restrained to indicate the location of auditory and visual targets via eye position. Long-duration visual targets were localized accurately with little error, but the locations of short-duration visual and both long- and short-duration auditory targets were markedly underestimated. With the head unrestrained, localization accuracy improved substantially for all stimuli and all durations. While the improvement for long-duration stimuli with the head unrestrained might be expected given that dynamic sensory cues were available during the gaze shifts and the lack of a memory component, surprisingly, the improvement was greatest for the auditory and visual stimuli with the shortest durations, where the stimuli were extinguished prior to the onset of the eye or head movement. The underestimation of auditory targets with the head restrained is explained in terms of the unnatural sensorimotor conditions that likely result during head restraint.