The owl’s brain is a showcase in Systems Neuroscience for allowing the analytical approach to how information is processed and represented in the brain. Owls exhibit a characteristic orienting response towards sound sources. This behavior is highly reproducible, the variables involved in triggering specific responses are well characterized, and the system affords progressively deeper levels of analysis. Whereas spatial selectivity of neurons in the owl’s auditory system is initially broad and ambiguous, sharp space-specificity emerges in high-order neurons. In the midbrain, a map of auditory space is computed based on differences in time and intensity of the acoustic signals that arrive at each ear. These binaural cues are processed in parallel pathways that converge where the map emerges. We have focused on regions of the brain that are crucial for this synthetic process: the neurons where the difference between the arrival times of the sound to each ear is initially detected, and the space-specific neurons that respond to sounds coming from unique directions. We found that well-defined computations, which match predictions made by studies of sound localization in humans, underlie the emergent response properties of these neurons. Thus, the owl’s brain provides a system to test models of psychoacoustics at levels from single cells to networks of neurons.

In recent years, we have studied owls' behavioral biases when localizing sounds. We could predict these biases by statistical inference implemented in the owl’s brain. We have recently developed recording of neuronal populations in both anesthetized and awake animals, experience dependen changes and started a collaboration with the Sussman laboratory at Einstein to test hypotheses raised by our work in barn owls, in human spatial perception.

Shadron K, Pena JL (2023) Development of frequency tuning shaped by spatial cue reliability in the barn owl's auditory midbrain. eLife, 12:e84760..

Ferger R, Shadron K, Fischer BJ, Pena JL (2021) Barn Owl's Auditory Space Map Activity Matching Conditions for a Population Vector Readout to Drive Adaptive Sound Localizing Behavior. J. Neurosci. 41(50):10305-10315.

Pavao R, Sussman ES, Fischer BJ, Pena JL (2020) Natural ITD statistics predict human auditory spatial perception eLife, 9:e51927.

Beckert MV, Fischer BJ, Pena JL (2020) Effect of stimulus-dependent spike timing on population coding of sound location in the owl’s auditory midbrain. eNeuro, 7(2) ENEURO.0244-19.2020 1–21.

Pena JL, Cazettes F, Beckert MV, Fischer BJ (2019) Viewpoint: Synthesis of hemispheric ITD tuning from the readout of a neural map: commonalities of proposed coding schemes in birds and mammals. Journal of Neuroscience, 39: 9053-9061.

Cazettes F, Fischer BJ, Beckert MV, Pena JL (2018) Emergence of an adaptive command for orienting behavior in premotor brainstem neurons of barn owls. Journal of Neuroscience, http://www.jneurosci.org/content/early/2018/07/16/JNEUROSCI.0947-18.2018

Batista G, Johnson JL, Dominguez E, Costa-Mattioli M, Pena JL (2018) Regulation of filial imprinting and structural plasticity by mTORC1 in newborn chickens. Scientific Reports, https://www.nature.com/articles/s41598-018-26479-1

Beckert MV, Pavao R, Pena JL (2017) Distinct correlation structure supporting a rate-code for sound localization in the owl's auditory forebrain. eNeuro, https://doi.org/10.1523/ENEURO.0144-17.2017.

Batista G, Johnson JL, Dominguez E, Costa-Mattioli M, Peña JL. (2016) Translational control of auditory imprinting and structural plasticity by eIF2α. eLife. Dec 23; 5:e17197.

Fischer BJ, Peña JL (2016) Optimal nonlinear cue integration for sound localization. J Comput Neurosci. 2016 Oct 6.

Cazettes F, Fischer BJ, Peña JL (2016) Cue Reliability Represented in the Shape of Tuning Curves in the Owl's Sound Localization System. J Neurosci. 2016 Feb 17;36(7):2101-10.

Rich D, Cazettes F, Wang Y, Peña JL, Fischer BJ (2015) Neural representation of probabilities for Bayesian inference. J Comput Neurosci. 38(2):315-23.

Cazettes F, Fischer BJ, Peña JL (2014) Spatial cue reliability drives frequency tuning in the barn Owl's midbrain. Elife. 3:e04854.

Fontaine B, Köppl C, Peña JL (2015) Reverse correlation analysis of auditory-nerve fiber responses to broadband noise in a bird, the barn owl. J Assoc Res Otolaryngol. 16(1):101-19.

Fontaine B, MacLeod KM, Lubejko ST, Steinberg LJ, Köppl C, Peña JL. (2014) Emergence of band-pass filtering through adaptive spiking in the owl's cochlear nucleus. J Neurophysiol. 112(2):430-45.

Wang Y, Gutfreund Y, Peña JL (2014) Coding space-time stimulus dynamics in auditory brain maps. Front Physiol. 5:135.

Fontaine B, Peña JL, Brette R (2014) Spike-threshold adaptation predicted by membrane potential dynamics in vivo. PLoS Comput Biol. 10(4):e1003560.

Peña JL, Gutfreund Y. (2014) New perspectives on the owl's map of auditory space. Curr Opin Neurobiol. 24(1):55-62.

Wang Y, Peña JL (2013) Direction selectivity mediated by adaptation in the owl's inferior colliculus. J Neurosci. 33(49):19167-75.

Steinberg LJ, Fischer BJ, Peña JL (2013) Binaural gain modulation of spectrotemporal tuning in the interaural level difference-coding pathway. J Neurosci. 33(27):11089-99.

Wang Y, Shanbhag SJ, Fischer BJ, Pena JL (2012) Population-wide bias of surround suppression in auditory spatial receptive fields of the owl’s midbrain. J. Neurosci. 32: 10470–8.

Fischer BJ, Steinberg LJ, Fontaine B, Brette R, Pena JL (2011) Effect of instantaneous frequency glides on ITD processing by auditory coincidence detectors. Proc Nat Acad Sci USA. 108: 18138–43.

Fischer BJ, Pena JL (2011) Owl’s behavior and neural representation predicted by Bayesian inference. Nat. Neurosci. 14: 1061–1066.

Penzo MA, Peña JL (2011) Depolarization-induced suppression of spontaneous release in the avian midbrain. J. Neurosci. 31: 3602–9.

Steinberg LJ, Peña JL (2011) Difference in response reliability predicted by spectrotemporal tuning in the cochlear nuclei of barn owls. J. Neurosci. 31: 3234–42.

Peña JL, DeBello (2010) Auditory processing, plasticity, and learning in the barn owl. ILAR Journal. 51: 338–52.

Fischer BJ, Anderson CH, Peña JL (2009) Multiplicative auditory spatial receptive fields created by a hierarchy of population codes. PLoS One. 4: e8015.

Perez ML, Shanbhag SJ, Peña JL (2009) Auditory spatial tuning at the cross-roads of the midbrain and forebrain. J. Neurophys. 102:1472–82.

Fischer BJ, Peña JL (2009) Bilateralmatching of frequency tuning in neural cross-correlators of the owl. Biol Cybern. 100:521–531.

Penzo MA, Peña JL (2009) Endocannabinoid-mediated long-term depression in the avian midbrain expressed presynaptically and postsynaptically. J. Neurosci. 29:4131–4139.

Fischer BJ, Christianson GB, Peña JL (2008) Cross-correlation in the auditory coincidence detectors of owls. J. Neurosci. 28: 8107–8115.

Wild JM, Kubke MF, Peña JL (2008) A pathway for predation in the brain of the barn owl (Tyto alba): projections of the gracile nucleus to the “claw area” of the rostral wulst via the dorsal thalamus. J. Comp. Neurol. 509:156–66.