1. Visually-induced auditory spatial adaptation in monkeys and humans Norbert Kopčo Center for Cognitive Neuroscience, Duke University Hearing Research Center, Boston University Technical University of Košice, Slovakia (Frequent flier # OK10509496)

2. 2 of 27 Nov 2, 2007BU HRC Introduction Visual stimuli can affect the perception of sound location e.g. the Ventriloquism Effect Way to go Red Sox! Way to go Red Sox! But does effect persist?

3. 3 of 27 Nov 2, 2007BU HRC Introduction Visual stimuli can affect the perception of sound location e.g. the Ventriloquist Effect Way to go Red Sox! But does effect persist? - barn owls: prism adaptation (Knudsen et al.) - monkeys: “ventriloquism aftereffect” (Woods and Recanzone, Curr. Biol. 2004) Why does the effect persist? Calibration of auditory perception (on different time scales): - to new environments (rooms) - to anatomical changes (head size)

4. 4 of 27 Nov 2, 2007BU HRC GOALS 1. Ventriloquism “aftereffect” in saccade task, in monkeys and humans? - well-defined sensory-motor paradigm - bridge to barn owl prism adaptation studies (on different time scale) 2. Reference frame of plasticity? - Visual, auditory, or oculomotor reference frame?

5. 5 of 27 Nov 2, 2007BU HRC Methods Basic idea: 1. Pre-adaptation baseline: Measure auditory saccade accuracy 2. Adaptation phase: Present combined visual-auditory stimuli, with visual location shifted 3. Compare auditory saccade accuracy pre- and post-adaptation

6. 6 of 27 Nov 2, 2007BU HRC Methods Initial experiment: Does it work? Design: Monkey Pre-adaptation baseline – ~100 Auditory-only trials Adaptation phase – 80% V-A stimuli, visual stimulus shifted 6 deg. Left or Right 20% Auditory-only Compare Auditory-only trials from adaptation phase to pre- adaptation phase Sounds: Loudspeakers Visual stimuli: LEDs

7. 7 of 27 Nov 2, 2007BU HRC RESULTS

8. 8 of 27 Nov 2, 2007BU HRC RESULTS

9. 9 of 27 Nov 2, 2007BU HRC RESULTS

10. 10 of 27 Nov 2, 2007BU HRC RESULTS

11. 11 of 27 Nov 2, 2007BU HRC QUESTION How does vision calibrate sound perception in primates? - monkeys and humans Unlike barn owls, monkeys and humans make eye movements. With every eye movement, the relationship between visual space and auditory space changes. Visual and auditory spatial information are different!

12. 12 of 27 Nov 2, 2007BU HRC Visual and auditory spatial information are different! VISION: Retina provides “map” of object locations Locations shift when eyes move Frame of reference is “eye- centered”

13. 13 of 27 Nov 2, 2007BU HRC Visual and auditory spatial information are different! AUDITORY: Sound location calculated from interaural timing and level differences Cue values do NOT shift when eyes move Frame of reference is “head- centered”

14. 14 of 27 Nov 2, 2007BU HRC Goals Eye-centered? Head (ear) -centered? Oculomotor? ? ? Perform behavioral experiments to answer the following questions: Does visual calibration of auditory space occur in eye-centered, head-centered, or a hybrid coordinate system? Are humans and monkeys similar?

15. 15 of 27 Nov 2, 2007BU HRC Experimental Setup Audiovisual display as viewed by the subject Horizontal location (degrees) Vertical location (degrees) 9 speakers in front of listener (~1 m distance), separated by 7.5° (humans) or 6° (monkeys) Light-emitting diodes (LEDs) at three center speakers: - aligned with speakers, or - displaced to the left or to the right (by 5°-humans, 6°-monkeys) 2 LEDs below speaker array used as fixation points (FP) Stimuli: Auditory stimulus: 300-ms broadband noise burst Audio-Visual stimulus: Same noise with synchronously lid LED.

16. 16 of 27 Nov 2, 2007BU HRC Method Audiovisual display Expected behavior Stimulus Location (°) Magnitude (°) Induce shift: - in only one region of space - from a single fixation point Test to see if shift generalizes to the same sub-region in: - head-centered space - eye-centered space

17. 17 of 27 Nov 2, 2007BU HRC Experiment: Procedure Audiovisual display as viewed by the subject Horizontal location (degrees) Vertical location (degrees) One trial consists of: 1. Fixation point (FP) appears. 2. Subject fixates FP. 3. Target stimulus is presented (Audio-Visual or Auditory-only). 4. Subject saccades to perceived location of stimulus (humans instructed to always saccade to sound). 5. Monkeys only: Reward for responding within a criterion window (+- 10° from speaker).

18. 18 of 27 Nov 2, 2007BU HRC Experiment: Procedure Experiment divided into 1-hour blocks. AV stimulus type kept constant within a block (left, right, or no displacement). 12 blocks for humans, 16 for monkeys. Subjects: 7 humans, 2 monkeys. Within a block three types of trials, randomly interleaved: AV FP on left and right. In presentation collapsed to right. AV stimuli 50 % of trials FP LEDs Speakers A-only stimuli trained FP: 25% of trials A-only stimuli shifted FP: 25% of trials

19. 19 of 27 Nov 2, 2007BU HRC Results: Humans Audiovisual display Expected Responses FP LEDs Speakers Stimulus Location (°) Induced Shift Magnitude (M+SE °) or Trained FP A-only responses: - Shift induced in trained sub-region - Generalization to untrained regions (asymmetrical) Shifted FP A-only responses: - Shift reduced in center region Head-centered representation, modulated by eye position

20. 20 of 27 Nov 2, 2007BU HRC Results: Monkeys Audiovisual display Expected Responses FP LEDs Speakers Stimulus Location (°) Magnitude of Induced Shift (°) or Trained FP A-only responses: - Shift in trained sub- region weaker - Generalization to untrained regions stronger (asymmetry oppo- site to humans) Shifted FP A-only responses: - Shift decreases on the right - Shift increases on the left Humans: Representation more mixed than in humans

21. 21 of 27 Nov 2, 2007BU HRC Summary The main results are consistent across species: Locally induced ventriloquist effect results in short-term adaptation, causing 30-to-50% shifts in responses to A-only stimuli from trained sub-region. The induced shift generalizes outside the trained sub-region, with gradually decreasing strength (However, the pattern of generalization differs across the species) The pattern of induced shift changes as the eyes move. But, overall, it appears to be in a representation frame that is more head-centered than eye-centered.

22. 22 of 27 Nov 2, 2007BU HRC Discussion (almost done) Posterior Parietal Cortex Neural adaptation could have been induced at several stages along the pathway (IC, MGB, AC, PPX, MC, SC). In humans, multiple effects observed at different temporal scales  likely adaptation at multiple stages Future work Examine temporal and spatial factors influencing the eye- centered modulation. Look at other trained sub-regions. Midbrain Pons Cerebrum Thalamus Midbrain Pons Thalamus (Kandel, Schwartz, Jessel) and (Purves)

23. 23 of 27 Nov 2, 2007BU HRC Humans: temporal profile In humans, multiple effects observed at different temporal scales  likely adaptation at multiple stages FP LEDs Speakers

24. 24 of 27 Nov 2, 2007BU HRC Humans: ipsilateral shift FP LEDs Speakers Eye-centered modulation does not occur. Possible explanation: the modulation is specific to the eye-centered hemisphere in which the audiovisual shift is induced (I-Fan currently testing)

25. 25 of 27 Nov 2, 2007BU HRC Monkeys: central vs. ipsi shift FP LEDs Speakers FP LEDs Speakers Are the monkeys really adapting in an eye-centered co-ordinate frame?

26. 26 of 27 Nov 2, 2007BU HRC Summary The main results are consistent across species (when shift induced in CENTER): Shift induced in the center Shift generalizes to non-trained sub-regions Shift changes with eye movement The consistency across species is less obvious when the trained sub-region shifts to IPSI: Humans: The relatively small eye modulation disappears Monkeys: Eye movement induces shift that is almost purely eye- centric

27. Jennifer Groh Center for Cognitive Neuroscience, Duke University I-Fan Lin Barbara Shinn-Cunningham Hearing Research Center, Boston University Support NIH grants to Barb and Jenni Slovak Science Grant Agency Collaborators