Tonotopic organization in the avian telencephalon

Organisms use their sensory systems to acquire information from their environment and integrate this information to produce relevant behaviors. Nevertheless, how sensory information is converted into adequate motor patterns in the brain remains an open question. Here, we addressed this question using two-photon and light-sheet calcium imaging in intact, behaving zebrafish larvae. We monitored neural activity elicited by auditory stimuli while simultaneously recording tail movements. We observed a spatial organization of neural activity according to four different response profiles (frequency tuning curves), suggesting a low-dimensional representation of frequency information, maintained throughout the development of the larvae. Low frequencies (150–450 Hz) were locally processed in the hindbrain and elicited motor behaviors. In contrast, higher frequencies (900–1,000 Hz) rarely induced motor behaviors and were also represented in the midbrain. Finally, we found that the sensorimotor transformations in the zebrafish auditory system are a continuous and gradual process that involves the temporal integration of the sensory response in order to generate a motor behavior.

Topographic organization is a hallmark of sensory cortical organization. Topography is robust at spatial scales ranging from hundreds of microns to centimeters, but can dissolve at the level of neighboring neurons or subcellular compartments within a neuron. This dichotomous spatial organization is especially pronounced in the mouse auditory cortex, where an orderly tonotopic map can arise from heterogeneous frequency tuning between local neurons. Here, we address a debate surrounding the robustness of tonotopic organization in the auditory cortex that has persisted in some form for over 40 years. Drawing from various cortical areas, cortical layers, recording methodologies, and species, we describe how auditory cortical circuitry can simultaneously support a globally systematic, yet locally heterogeneous representation of this fundamental sound property.

New neurons formed in the adult brain are incorporated into existing circuits. However, the number of new neurons recruited into a given brain region varies widely depending on the experience of the animal. An emerging general principle is that recruitment and early neuronal survival may be correlated with activity or use of the brain region. Here we show that use-dependent neuronal survival also occurs in the higher order auditory processing region of the songbird caudomedial nidopallium (NCM). We suggest that retention of young neurons may in part be influenced by use of the system without an increased demand for learning or behavioral plasticity.

The avian auditory system has become a model system to investigate how vocalizations are memorized and processed by the brain in order to mediate behavioral discrimination and recognition. Recent studies have shown that most of the avian auditory system responds preferentially and efficiently to sounds that have natural spectro-temporal statistics. In addition, neurons in secondary auditory forebrain areas have plastic response properties and are the most active when processing behaviorally relevant vocalizations. Physiological measurements show differential responses for vocalizations that were recently learned in discrimination tasks, and for the tutor song, a longer-term auditory memory that is used to guide vocal learning in male songbirds.

A miniature lightweight radio telemetric device is described which is shown to be suitable for recording neuronal activity in freely behaving animals. Its size (12 × 5 × 8 mm) and weight (1.0–1.1 g with batteries, 0.4–0.5 g without) make the device particularly suitable for recording neuronal units in small animals such as mice or zebra finches. The device combines a high impedance preamplifier, RC-filters and an FM-transmitter. Using the device we recorded action potentials in field L of freely behaving zebra finches (12–17 g) through chronically implanted tungsten electrodes. In freely behaving birds we observed frequency dependent responses of field L units to auditory stimuli for periods of up to 7 days. We investigated the effect of the device on singing and locomotor activity of the zebra finches. Singing and locomotion were significantly affected on the first day after surgery. Both anesthesia and the presence of the transmitter contributed to the observed effect. After 1 day of recovery, singing activity returned to 99.6% and perch-hopping activity to 55.3% of the baseline levels. It is concluded that the device is well suited for recording spike trains from small animals while they behave freely and naturalistically.

Recent literature on the Field L of songbirds, showing that some neurons present a clear selectivity towards complex sounds, especially conspecific songs, is reviewed. Furthermore, studies on European starlings have revealed a complex functional organization in this central auditory area, with subareas exhibiting different response features. Interestingly, both the functional organization and the neuronal specialization can be drastically affected by early deprivation, clearly showing the existence of a developmental plasticity. Some recovery seems to remain possible at later stages, and social factors may be involved.