Virtually all sensory experience occurs in the context of active behaviors

1. Virtually all sensory experience occurs in the context of active behaviors 1 2 3 4 5

2. Thesis: sensing and “sensing actions” are processed in a concerted fashion • Sensing actions involve moving the stimulus object with respect to the sense organ, or perturbing the stimulus object in some way. • In many cases, sensing actions are central to the task of collecting accurate information about the environment. • Knowledge of sensing actions can be critical to the interpretation of sensory signals.

3. Specializations of the retinal fovea: densest packing of photoreceptors and lowest convergence of photoreceptors onto ganglion cells http://webvision.med.utah.edu

4. Specializations of the retinal fovea: displacement of inner retina http://webvision.med.utah.edu

5. Specializations of the retinal fovea: absence of retinal vasculature http://webvision.med.utah.edu

6. Acute vision only occurs within a few degrees of the fovea Hans-Werner Hunziker, (2006) “Im Auge des Lesers”, Transmedia Stäubli Verlag Zürich

7. Saccadic eye movements bring objects into the fovea We make a saccade 2-3 times per second.

8. The problem with eye movements #1: Problem: eye movements create fictive motion of the image on the retina. Solution: the visual system interprets visual signals in the context of knowledge about coordinated eye movements. -- Hermann von Helmholtz, Physiologische Optik trans. William James, The Principles of Psychology

9. The problem with eye movements #2: Problem: eye movements blur the image on the retina. Solution: visual signals are suppressed during saccades. cat LGN, spontaneous saccades in the dark, avg of 71 cells Lee & Malpeli, J. Neurophysiol. 1998

10. The problem with eye movements #3: Problem: eye movements change the relationship between the visual world and the head, so visual and auditory maps are misaligned. Solution: eye position modifies the auditory receptive fields of superior colliculus neurons. Stein & Stanford 2008

11. The problem with head movements: Problem: head movements cause a stationary object to move out of the fovea. Solution: The eyes move precisely to oppose head movement. This is called the vestibular-ocular reflex (VOR). The gain of the VOR can be changed by pairing head movement with stimulus movement. Boyden, Katoh, & Raymond Annu. Rev. Neurosci. 2004

12. Hearing: localization acuity depends on source position Thus, head movements can “foveate” an auditory stimulus. human psychophysics Sabin, Macpherson , & Middlebrooks, Hearing Res. 2004

13. Hearing: self-sound is filtered differently from non-self sound A giant neuron conveys corollary discharge to auditory processing centers and transiently “deafens” the cricket. CDI morphology: Hedwig & Poulet Science 2006

14. Olfaction: sniffing is an active process Kepecs, Uchida, & Mainen J. Neurophysiol. 2007

15. Novel odors can trigger rapid increases in sniff rate rat Wesson et al., PloS Biology 2008

16. A two-alternative forced-choice paradigm for odor discrimination 2-alternative forced-choice w/ water reward Uchida & Mainen, Nat. Neurosci. 2003

17. Sniff rate increases in anticipation of an odor mouse 1 mouse 2 mouse 3 2-alternative forced-choice w/ water reward Wesson et al., Chem. Senses 2008

18. Rapid sniffing attenuates olfactory receptor neuron input to the olfactory bulb head-fixed rat, rat calcium imaging w/ OGB Verhagen et al., Nat. Neurosci. 2007

19. Effects of rapid sniffing are bottom-up (not top-down) head-fixed rat, rat calcium imaging w/ OGB Verhagen et al., Nat. Neurosci. 2007

20. Somatosensation: rodent whisking as a model for active encounters with somatosensory stimuli Kleinfeld, Ahissar, & Diamond, Curr. Opin. Neurobiol. 2006 Adapted from Fee, Mitra, & Kleinfeld, J. Neurophysiol. 1997

21. The whisker pad has a large representation in the somatosensory cortex of the rodent Petersen Pflugers Arch. 2003

22. Somatosensory cortex contains “reference signals” about whisker motion Crochet & Petersen, Nat. Neurosci. 2006 whole-cell patch-clamp recording from awake mouse

23. Responses to whisker deflection in barrel cortex depend on whether the animal is actively whisking Ferezou, Petersen et al, Neuron 2006

24. Somatosensory and motor circuits are linked by sensorimotor loops 4° 3° paralemniscal (motion) lemniscal (both) extralemniscal (touch) 2° motor neurons 1° Kleinfeld, Ahissar, & Diamond, Curr. Opin. Neurobiol. 2006

25. Electrosensation: sensory exotica Gnathonemus petersii see e.g., Sensory Exotica: A World beyond Human Experience, by H. Hughes (MIT Press, 2001)

26. higher brain regions electrosensory lobe (ELL) Active sensing in electrosensation electric organ discharge command nucleus electric organ electrosensory receptor neurons fish water electric organ discharge (EOD) adapted from Bell J. Exp. Biol. 1989

27. Active sensing in electrosensation The fish actively produces electric organ discharges (EODs). Objects in the water perturb the amplitude of the electric field. This changes the latency of spikes in electrosensory afferents.

28. higher brain regions electric organ corollary discharge (EOCD) local lidocaine electrosensory lobe (ELL) intramuscular curare metallic current sink electric organ discharge command nucleus electric organ electrosensory receptor neurons fish water electric organ discharge (EOD) adapted from Bell J. Exp. Biol. 1989

29. Plastic responses to corollary discharge EOD command (effect on the electric organ is blocked with curare) command alone command + electrosensory stimulus 1.5 msec later (9 min) command alone 1 min 80 msec recording from mormyrid ELL Bell Brain Res. 1986

30. higher brain regions electric organ corollary discharge (EOCD) electrosensory lobe (ELL) proprioceptors electric organ discharge command nucleus electric organ electrosensory receptor neurons fish water electric organ discharge (EOD) adapted from Bell J. Exp. Biol. 1989

31. Plastic responses to proprioceptive stimuli recording from gymnotid ELL Bastien J. Comp. Physiol. 1995