Hunting Increases Adaptive Auditory Map Plasticity in Adult Barn Owls

The midbrain contains an auditory map of space that is shaped by visual experience. When barn owls are raised wearing spectacles that horizontally displace the visual field, the auditory space map in the external nucleus of the inferior colliculus (ICX) shifts according to the optical displacement of the prisms. Topographic visual activity in the optic tectum could serve as the template that instructs the auditory space map. We studied the effects of a restricted, unilateral lesion in the portion of the optic tectum that represents frontal space. Here we show that such a lesion eliminates adaptive adjustments specifically in the portion of the auditory map that represents frontal space on the same side of the brain, while the rest of the map continues to adjust adaptively. Thus, activity in the tectum calibrates the auditory space map in a location-specific manner. Because the site of adaptive changes is the ICX, the results also indicate that the tectum provides a topographic instructive signal that controls adaptive auditory plasticity in the ICX.

The barn owl's optic tectum contains a map of auditory space that is based, in part, on a map of interaural time difference (ITD). Previous studies have shown that this ITD map is shaped by auditory experience. In this study, we investigated whether the plasticity responsible for experience-induced changes in ITD tuning in the tectum occurs within the tectum itself or at an earlier stage in the auditory pathway. We altered auditory experience in young owls by implanting an acoustic filtering device in one ear that caused frequency-dependent changes in sound timing and level. We analyzed the representation of ITD in normal and device-reared owls in two nuclei in the ascending pathway: the external nucleus of the inferior colliculus (ICX), the primary source of ascending auditory input to the tectum, and the lateral shell of the central nucleus of the inferior colliculus (ICCls), the primary source of input to the ICX. In the ICX, device rearing caused adaptive, frequency-dependent changes in ITD tuning, as well as changes in frequency tuning. These changes in tuning were similar to changes that occurred in the optic tectum in the same owls. In contrast, in the ICCls, tuning for ITD and frequency was unaffected by device rearing. The data indicate that plasticity at the level of the ICX is largely responsible for the adaptive adjustments in ITD tuning and frequency tuning that are observed in the optic tecta of owls raised with abnormal auditory experience.

Barn owls can localize a sound source using either the map of auditory space contained in the optic tectum or the auditory forebrain. The auditory thalamus, nucleus ovoidalis (N.Ov), is situated between these two auditory areas, and its inactivation precludes the use of the auditory forebrain for sound localization. We examined the sources of inputs to the N.Ov as well as their patterns of termination within the nucleus. We also examined the response of single neurons within the N.Ov to tonal stimuli and sound localization cues. Afferents to the N.Ov originated with a diffuse population of neurons located bilaterally within the lateral shell, core, and medial shell subdivisions of the central nucleus of the inferior colliculus. Additional afferent input originated from the ipsilateral ventral nucleus of the lateral lemniscus. No afferent input was provided to the N.Ov from the external nucleus of the inferior colliculus or the optic tectum. The N.Ov was tonotopically organized with high frequencies represented dorsally and low frequencies ventrally. Although neurons in the N.Ov responded to localization cues, there was no apparent topographic mapping of these cues within the nucleus, in contrast to the tectal pathway. However, nearly all possible types of binaural response to sound localization cues were represented. These findings suggest that in the thalamo-telencephalic auditory pathway, sound localization is subserved by a nontopographic representation of auditory space.

Throwing light on plasticity, with shades

The barn owl ( Tyto alba) is capable of capturing prey by passive hearing alone, guided by a topographic map of auditory space in the external nucleus of its inferior colliculus. The neurons of this auditory space map have discrete spatial receptive fields that result from the computation of interaural differences in the level (ILD) and time-of-arrival (ITD) of sounds. Below we review the synthesis of the spatial receptive fields from the frequency-specific ITDs and ILDs to which the neurons are tuned, concentrating on recent studies exploiting virtual auditory space techniques to analyze the contribution of ILD. We then compared the owl's spatial discrimination, assessed behaviorally, with that of its space map neurons. Spatial discrimination was assessed using a novel paradigm involving the pupillary dilation response (PDR), and neuronal acuity was assessed by measuring the changes in firing rate resulting from changes in source location, scaled to the variance. This signal-detection-based approach revealed that the change in the position of the neural image on this map best explains the spatial discrimination measured using the PDR. We compare this result to recent studies in mammalian systems.

Sensory systems preferentially strengthen responses to stimuli based on their reliability at conveying accurate information. While previous reports demonstrate that the brain reweighs cues based on dynamic changes in reliability, how the brain may learn and maintain neural responses to sensory statistics expected to be stable over time is unknown. The barn owl's midbrain features a map of auditory space where neurons compute horizontal sound location from the interaural time difference (ITD). Frequency tuning of midbrain map neurons correlates with the most reliable frequencies for the neurons' preferred ITD (Cazettes et al., 2014). Removal of the facial ruff led to a specific decrease in the reliability of high frequencies from frontal space. To directly test whether permanent changes in ITD reliability drive frequency tuning, midbrain map neurons were recorded from adult owls, with the facial ruff removed during development, and juvenile owls, before facial ruff development. In both groups, frontally tuned neurons were tuned to frequencies lower than in normal adult owls, consistent with the change in ITD reliability. In addition, juvenile owls exhibited more heterogeneous frequency tuning, suggesting normal developmental processes refine tuning to match ITD reliability. These results indicate causality of long-term statistics of spatial cues in the development of midbrain frequency tuning properties, implementing probabilistic coding for sound localization.

How Hearing Happens

Whether the auditory and visual systems use a similar coding strategy to represent motion direction is an open question. We investigated this question in the barn owl's optic tectum (OT) testing stimulus-specific adaptation (SSA) to the direction of motion. SSA, the reduction of the response to a repetitive stimulus that does not generalize to other stimuli, has been well established in OT neurons. SSA suggests a separate representation of the adapted stimulus in upstream pathways. So far, only SSA to static stimuli has been studied in the OT. Here, we examined adaptation to moving auditory and visual stimuli. SSA to motion direction was examined using repeated presentations of moving stimuli, occasionally switching motion to the opposite direction. Acoustic motion was either mimicked by varying binaural spatial cues or implemented in free field using a speaker array. While OT neurons displayed SSA to motion direction in visual space, neither stimulation paradigms elicited significant SSA to auditory motion direction. These findings show a qualitative difference in how auditory and visual motion is processed in the OT and support the existence of dedicated circuitry for representing motion direction in the early stages of visual but not the auditory system.

In the process of Printing the article “Sound-Localization Deficits Induced by Lesions in the Barn Owl's Auditory Space Map,” by Hermann Wagner [J Neurosci13:371–386 (1993)] the scale bar belonging to the photographs of Fig. 4 (p. 376) was lost. The scale bar belonging to Fig. 3 (p. 375) is valid for Figure 4,b, d, f,andh,as well. The publisher regrets the error.

I investigated the neural algorithms by which neurons gain selectivity for interaural level difference in the brainstem of the barn owl (Tyto alba). Differences in the timing and in the level of sounds at the ears are used by this owl to encode, respectively, azimuthal and vertical position of sound sources in space. These two cues are processed in two parallel neural pathways. Below the level of the inferior colliculus, all neurons in the pathway that processes level differences show responses to this cue that are monotonic, and thus not selective for a particular level difference. Only in the inferior colliculus, which contains a map of auditory space, are neurons sharply tuned to specific interaural level differences. How are these response properties generated from those of the nuclei that provide input to the inferior colliculus? I show that the posterior subdivision of the nucleus ventralis lemnisci lateralis (VLVp) projects bilaterally to the lateral shell of the central nucleus of the inferior colliculus, the input stage to the map of auditory space. Both these nuclei are part of the pathway that processes interaural level differences. Manipulations of the responses in VLVp affected the responses to level differences in the inferior colliculus; responses to time differences were unaffected. By systematically increasing or decreasing neural activity in VLVp, I show that the VLVp on each side provides inhibition to the colliculus at large level differences. This results in a peaked response that is tuned to level differences in the inferior colliculus. Some cells in the lateral shell of the inferior colliculus appear to receive direct GABAergic inhibition from VLVp. I suggest that this circuitry and the algorithms it supports are the neural substrates that allow the barn owl to exploit level differences for computation of sound source elevation.

Echoes that arrive after short delays are not perceived as events separate from sounds arriving directly from an active source, a phenomenon known as localization dominance. Studies have focused on the time-advantage at the onset of an echo/direct-sound pair to explain localization dominance. The head-saccades of barn owls and the responses of neurons in their auditory space maps were measured when sound pairs were gated simultaneously, so that the lead/lag relationship could be discerned only from the ongoing features of the envelopes. The owls behaved as though they experienced localization dominance at short delays, but only if the sounds were deeply amplitude modulated, suggesting the importance of the ongoing envelope. Correspondingly, neurons in the space map fired preferentially to the leading sound, thus paralleling the behavior, but again, deep amplitude modulations were necessary. Analyses of waveforms at the ears suggest that the acoustic features that caused the space map neurons to fire were more abundant for the leading than for the lagging stimuli, thus explaining localization dominance without the need for explicit echo-suppression circuitry. [Work supported by NIDCD F32-DC008267 and RO1-DC003925.]

Barn owls enable investigation of neural mechanisms underlying stimulus selection of concurrent stimuli. The audiovisual space map in the optic tectum (OT), avian homolog of the superior colliculus, encodes relative strength of concurrent auditory stimuli through spike response rate and interneuronal spike train synchrony (STS). Open questions remain regarding stimulus selection in downstream forebrain regions lacking topographic coding of auditory space, including the functional consequences of interneuronal STS on interregional signaling. To this end, we presented concurrent stimuli at different locations and manipulated relative strength while simultaneously recording neural responses from OT and its downstream thalamic target, nucleus rotundus (nRt), in awake barn owls of both sexes. Results demonstrated that broadly spatially tuned nRt units exhibit different spike response patterns to competition depending on spatial tuning preferences. Modeling suggests nRt units integrate convergent inputs from distant locations across midbrain map regions. Additionally, STS within nRt reflects the temporal properties of the strongest stimulus. Furthermore, interregional STS between OT and nRt was strongest when spatial tuning overlap between units across regions was large and when the strongest stimulus location during competition was favorable for units in both regions. Additionally, though gamma oscillations synthesized within OT are weakly propagated within nRt, average gamma power across regions correlates with strength of interregional STS. Overall, we demonstrate that nRt integrates inputs across distant areas of OT, retains spatial information through differences in strength of inputs from various locations of the midbrain map across neurons, and prioritizes coding of identity features to the strongest sound.

The barn owl's midbrain and forebrain contain neurons tuned to sound direction. The spatial receptive fields of these neurons result from sensitivity to combinations of interaural time (ITD) and level (ILD) differences over a broad frequency range. While a map of auditory space has been described in the midbrain, no similar topographic representation has been found in the forebrain. The first nuclei that belong exclusively to the forebrain and midbrain pathways are the thalamic nucleus ovoidalis (Ov) and the external nucleus of the inferior colliculus (ICx), respectively. The midbrain projects to the auditory thalamus before sharp spatial receptive fields emerge; although Ov and ICx receive projections from the same midbrain nuclei, they are not directly connected. We compared the spatial tuning in Ov and ICx. Thalamic neurons respond to a broader frequency range and their ITD and ILD tuning varied more across frequency. However, neurons in Ov showed spatial receptive fields as selective as neurons in ICx. Thalamic spatial receptive fields were tuned to frontal and contralateral space and correlated with their tuning to ITD and ILD. Our results indicate that spatial tuning emerges in both pathways by similar combination selectivity to ITD and ILD. However, the midbrain and the thalamus do not appear to repeat exactly the same processing, as indicated by the difference in frequency range and the broader tuning to binaural cues. The differences observed at the initial stages of these sound-localization pathways may reflect diverse functions and coding schemes of midbrain and forebrain.

A region in the barn owl forebrain, referred to as the archistriatal gaze fields (AGF), is shown to be involved in auditory orienting behavior. In a previous study, electrical microstimulation of the AGF was shown to produce saccadic movements of the eyes and head, and anatomical data revealed that neurons in the AGF region of the archistriatum project directly to brainstem tegmental nuclei that mediate gaze changes. In this study, we investigated the effects of AGF inactivation on the auditory orienting responses of trained barn owls. The AGF and/or the optic tectum (OT) were inactivated pharmacologically using the GABAA agonist muscimol. Inactivation of the AGF alone had no effect on the probability or accuracy of orienting responses to contralateral acoustic stimuli. Inactivation of the OT alone decreased the probability of responses to contralateral stimuli, but the animals were still capable of orienting accurately toward stimuli on about 60% of the trials. Inactivation of both the AGF and the OT drastically decreased the probability of responses to 16-21% and, on the few trials that the animals did respond, there was no relationship between the final direction of gaze and the location of the stimulus. Thus, with the AGF and OT both inactivated, the animals were no longer capable of orienting accurately toward acoustic stimuli located on the contralateral side. These data confirm that the AGF is involved in gaze control and that the AGF and the OT have parallel access to gaze control circuitry in the brainstem tegmentum. In these respects, the AGF in barn owls is functionally equivalent to the frontal eye fields in primates.

The natural acoustical environment contains many reflective surfaces that give rise to echoes, complicating the task of sound localization and identification. The barn owl (Tyto alba), as a nocturnal predator, relies heavily on its auditory system for tracking and capturing prey in this highly echoic environment. The external nucleus of the owl's inferior colliculus (ICx) contains a retina-like map of space composed of "space-specific" auditory neurons that have spatially limited receptive fields. We recorded extracellularly from individual space-specific neurons in an attempt to understand the pattern of activity across the ICx in response to a brief direct sound and a simulated echo. Space-specific neurons responded strongly to the direct sound, but their response to a simulated echo was suppressed, typically, if the echo arrived within 5 ms or less of the direct sound. Thus we expect there to be little or no representation within the ICx of echoes arriving within such short delays. Behavioral tests using the owl's natural tendency to turn their head toward a sound source suggested that owls, like their space-specific neurons, similarly localize only the first of two brief sounds. Naive, untrained owls were presented with a pair of sounds in rapid succession from two horizontally-separated speakers. With interstimulus delays of less than 10 ms, the owl consistently turned its head toward the leading speaker. Longer delays elicited head turns to either speaker with approximately equal frequency and in some cases to both speakers sequentially.