Adaptive plasticity in the auditory localization pathway of the barn owl

1. Adaptive plasticity in the auditory localization pathway of the barn owl Presentation of research from the lab of Eric I. Knudsen

3. Barn owl outer ear anatomy

4. Relationship of sound localization cue values and locations in space.

5. Auditory localization pathway LAM-nucleus laminaris MSO-medial superior olive VLVp-posterior division of ventral nucleus of lateral lemniscus Timing of cues is mapped in the LAM. Relative level of sounds is mapped is measured by frequency tuned neurons in the VLVp. Both binaural and monaural information ascends to central nucleus of inferior colliculus. From this point a major component goes to the thalamus and from there to auditory fields in the forebrain. A minor component remains in the midbrain in projecting to the external nucleus of the inferior colliculus (ICX).Timing of cues is mapped in the LAM. Relative level of sounds is mapped is measured by frequency tuned neurons in the VLVp. Both binaural and monaural information ascends to central nucleus of inferior colliculus. From this point a major component goes to the thalamus and from there to auditory fields in the forebrain. A minor component remains in the midbrain in projecting to the external nucleus of the inferior colliculus (ICX).

6. Mapping in inferior colliculus In the ICX frequency specific ITD and ILD information converges across frequency channels in the process of synthesizing a map of space. This information goes to the optic tectum where it merges with a visual map of space.

7. Auditory localization Interrupting flow of information on either branch leaves animal still able to orient to sound sources. Interrupting both pathways eliminates that ability. The midbrain localization pathway is responsible for orienting gaze in response to higher level commands. The forebrain localization pathway is responsible for higher order functions such as remembering previous sounds or coordinating complex behaviors.

8. Abnormal auditory experience Monaural occlusion leads to misjudging location of auditory stimuli in the direction of the unplugged ear. Owls eventually recover accurate sound localization with the earplug in place. Errors are not corrected if a blinder is placed over the eyes. Owls raised with one ear plugged and with displacing prisms adjust sound localization when the earplug is removed.

9. Vision is instructive in auditory spatial cues Owl with prisms. Auditory orienting responses are adjusted according to the optical displacement. Prisms alter the movement required to bring an auditory stimulus onto the center of the visual field.

10. Adjustment of auditory orienting response Data points indicate orientation of the head in response to auditory stimuli. Leads to visuomotor adjustments in areas such as extension of talons.

11. Effect of prism experience on auditory receptive field in OT

12. Shift of auditory tuning: Functional traces of learning

13. Functional traces of learning The shift involves : Learned responses—acquisition of neuronal responses to values of ITD that are adaptive with the prisms in place. Normal responses—elimination of responses to values of ITD that were previously effective but are no longer appropriate.

14. Neuronal ITD tuning in the ICX Measurements are from the same area in ICX and represent acquired learned responses to visually instructed range of ITDs. Normal response is eliminated over time.

15. Sensitive periods for ITD tuning in OT Shift in ITD tuning as a function of age. The sensitive period opens at 60 days when eyes have matured and closes at 200 days.

16. Effects of juvenile experience on capacity to adjust ITD tuning Prism experience leaves an enduring trace, allowing the owl to re-establish the abnormal map later in adulthood. Recovery of map is more complete in animals housed in an enriched environment.

17. Anatomical traces of learning in the ICX Axonal density is significantly greater in prism reared adults, although axonal density does not change within normal projection field. Biocytin was injected into a site representing 20micros ITD contralateral ear leading. This figure illustrates the expansion of this field when prisms are applied.Biocytin was injected into a site representing 20micros ITD contralateral ear leading. This figure illustrates the expansion of this field when prisms are applied.

18. Anatomical reorganization of projections from ICC to ICX as a result of prism experience

19. Schematic anatomical changes in the auditory space map Prismatic displacement leads to Abnormal rostral projection of ICC axons on one side (red) Abnormal caudal projection on the other. Normal projects persist (gray)

20. Pharmacological traces of learning Blocking NMDA receptors reduced auditory responses by 50% across entire range ITDs In prism reared owls Blocking NMDA receptors can eliminate learned responses.

21. Pharmacological traces of learning Injection of CNQX a non-NMDA receptor antagonist preferentially blocked normal response but not learned response. NMDA receptors mediate the expression of newly learned responses. (Different than LTP in CA1.)

22. Pharmacological traces of learning GABAA receptors suppress inappropriate normal responses in ICX. GABAA receptor antagonist bicuculline allows expression of normal responses. Iotophoretic injection of bicuculline at an ICX site that is expressing a fully shifted ITD tuning curve in owls that were at the late stage of learning leads to reexpression of a strong normal response.Iotophoretic injection of bicuculline at an ICX site that is expressing a fully shifted ITD tuning curve in owls that were at the late stage of learning leads to reexpression of a strong normal response.

23. Summary Functional and anatomical plasticity occurs in the inferior colliculus in response to altering visual input. Changes can be enhanced by an enriched environment. More profound changes occur during sensitive periods. Traces of the changes persist into adulthood. Low level of competition between alternative pathways in the inferior colliculus may be critical for retention of alternative maps.

24. Plasticity in response to removal of external ears

25. Influence of environmental richness on sensitive periods for adjustment of auditory orienting accuracy in response to prism experience.

26. Endurance of traces in the midbrain