Sensing and expectation

1. Sensing and expectation

2. Life is uncertain. Optimal statistical inference in an uncertain world requires that we integrate new information into a framework of prior expectations.

3. Suppose your patient has just tested positive for a disease. How likely is it that he actually has the disease? What factors do we need to consider? The probability of testing positive if you have the disease. The probability of testing positive if you are healthy. The probability that anybody has the disease, regardless of their test.

4. Thomas Bayes 1701?-1761 Bayes’ rule: The probability of sickness, given the result. The probability of the result, given sickness. The probability of sickness. The probability of the result.

5. Suppose your patient has just tested positive for a disease. How likely is it that he actually has the disease? • Consider this scenario: • the probability of testing positive if you have the disease is 95%, • the probability of testing positive if you are healthy is 5%, • but the disease is rare, so the probability that anybody has it is 1%.

6. Thomas Bayes 1701?-1761 Bayes’ rule: The probability of the stimulus after taking into account the response (the posterior distribution). The probability of the response after taking into account the stimulus. The probability of the stimulus occurring (the prior distribution). The probability of the response occurring.

7. eye movements head movements hand movements Sensing often occurs within the context of motor actions. Motor actions create expectations that are important for the optimal interpretation of sensory signals.

8. How does the nervous system account for the expected consequences of motor actions? 1. Solving this problem can involve filtering out the expected (“trivial”) consequences of motor actions. 2. Solving this problem can involve also performing a coordinate transform to re-register sensory information within a more stable coordinate system that is invariant to the motor action. Studying how the nervous system integrates sensory information with the expected consequences of motor actions provides a concrete way to study the integration of new information with prior expectations.

9. Filtering out the expected consequences of motor actions

10. Hearing: filtering out “expected” sounds wing nerve neuron carrying corollary discharge auditory neuron A dedicated single neuron in the cricket conveys corollary discharge to auditory processing centers and inhibits auditory interneurons when the cricket is singing. Hedwig & Poulet Science 2006

11. Vision: We move our eyes because our vision is poor outside the fovea Visual acuity (normalized) Hans-Werner Hunziker, (2006) “Im Auge des Lesers”, Transmedia Stäubli Verlag Zürich

12. Saccadic eye movements bring objects into the fovea We make a saccade several times per second.

13. Vision: filtering out “expected” visual motion Problem #1: fast (saccadic) 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

14. -- Hermann von Helmholtz, Physiologische Optik trans. William James, The Principles of Psychology Vision: filtering out “expected” visual motion Problem #2: even slow 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.

15. Electrosensation: filtering out “expected” electric field disruptions a “weakly electric fish”: Gnathonemus petersii see e.g., Sensory Exotica: A World beyond Human Experience, by H. Hughes (MIT Press, 2001)

16. 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

17. 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.

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

19. Plastic responses to corollary discharge in the electrosensory lobe EOD command (note: the effect on the electric organ has been blocked for several minutes 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

20. Plastic responses to corollary discharge recording from mormyrid ELL Bell Curr. Opin. Neurobiol. 2001

21. 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

22. Plastic responses to proprioceptive stimuli in the electrosensory lobe tail bend alone tail bend + electrosensory stimulus tail bend alone recording from gymnotid ELL Bastian J. Comp. Physiol. 19956

23. Parallel fiber synapses are the site of plasticity. A circuit for predicting the effects of sensing actions motor corollary discharge, proprioceptive afferents (i.e., the “expectation” signal) electroreceptive afferents (i.e., the sensory signal) mormyrid ELL Sawtell & Williams J. Neurosci. 2008

24. Coordinate transforms that re-register sensory information within a more stable coordinate system

25. The superior colliculus contains maps of auditory and visual space inter-aural level difference computed external nucleus of the inferior colliculus (map of auditory space) cochlear nuclei (bilateral) superior colliculus inter-aural time difference computed retina (map of visual space) Bimodal neurons in the superior colliculus have congruent receptive field locations.

26. Why might it be useful to map visual and auditory information onto the same coordinates? Multimodal neurons with congruent audio-visual receptive field locations trigger the same behavior even when one source of information is absent (e.g., if the prey is momentarily silent or out of sight). Auditory and visual information can be seamlessly combined when both are present, improving the estimate of the spatial location of the stimulus.

27. Vision and hearing: coordinate transforms Problem: eye movements change the relationship between the visual world and the head, so visual and auditory maps are misaligned. Solution: eye position transiently modifies the auditory receptive fields of superior colliculus neurons. Stein & Stanford Nature Neuroscience 2008

28. Vision and hearing: coordinate transforms Problem: the growth of the body changes the relationship between the world and the head, so visual and auditory maps can become misaligned over time. Solution: over time, eye position modifies the auditory receptive fields of superior colliculus (or tectum) neurons in a semi-stable fashion. www.ardgrain.com/barn-owls

29. day 1 of prisms (23º) visual auditory day 42 of prisms (23º) prisms removed visual visual auditory auditory Vision and hearing: coordinate transforms head turns evoked by visual or auditory stimuli in the barn owl before prisms visual auditory adapted from Knudsen & Knudsen 1989

30. Plasticity of auditory receptive fields in the owl tectum before → after prisms (23º) after 8 weeks of prisms

31. Why do auditory receptive fields shift toward visual receptive fields? If visual responses are stronger and/or more reliable, then a Hebbian mechanism is sufficient to explain this. before prisms just after prisms on after plasticity

32. Somatosensation: coordinate transforms Kleinfeld, Ahissar, & Diamond, Curr. Opin. Neurobiol. 2006 Adapted from Fee, Mitra, & Kleinfeld, J. Neurophysiol. 1997

33. Somatosensation: coordinate transforms A rodent can determine the position of an object relative to its head position through the use of a single moving vibrissa. This requires interpreting somatosensory information within the coordinate space dictated by vibrissa position. Curtis & Kleinfeld Nature Neuroscience 2009

34. Sensory encoding in rat S1 cortex depends on vibrissa position Primary somatosensory cortex neurons jointly encode both touch and whisking phase.

35. Sensory and motor circuits in the rodent whisking system are linked by multiple recurrent loops 4° 3° 2° motor neurons 1° Kleinfeld, Ahissar, & Diamond, Curr. Opin. Neurobiol. 2006