1
B. Liu, M.V. Macellaio and L.C. Osborne Rapid gain adaptation optimizes pursuit accuracy Department of Neurobiology, The University of Chicago, Chicago IL, USA 2. Rescaling of response gain with stimulus variance in MT neurons and pursuit: In the natural world, the statistics of sensory stimuli fluctuate across a wide range. In theory, the brain could maximize information recovery if sensory neurons adaptively rescale their sensitivity to match their limited response bandwidth to the current range of inputs. Such adaptive coding has been observed in a variety of systems, but the premise that adaptation optimizes behavior has not been tested. Here we show that adaptation in cortical sensory neurons maximizes information about visual motion, and minimizes tracking errors in pursuit eye movements guided by that cortical activity. Thus efficient sensory coding is not simply an ideal standard but rather a compact description of real sensory computation that manifests in improved behavioral performance. pursuit MT neuron a b I (bits) I mean (bits) n=23 0 0.5 1.5 -0.9 -0.6 -0.3 0 1 c d time (ms) -100 0 100 200 300 infomation (bits) 0 0.2 0.4 0.6 0.8 data shuffled -100 0 100 200 300 time (ms) infomation (bits) 0 0.1 0.2 0.3 0.4 data shuffled I normalized stimulus 1 0.5 0 -0.5 -1 normalized response 0 0.5 1 1/8 1/4 1/2 1 2 4 8 e f 0.125 1 8 gain scale factor normalized information MT (n=94) pursuit (n=7) 0 0.2 0.4 0.6 0.8 1 3. Mutual information: Maximize information by adaptive gain in MT neurons and pursuit. Rapid recovery of mutual information after step change in direction variance. probability d 0 10 20 30 a eye direction (deg) target direction (deg) 0 0.03 0.06 0.09 0.12 -30 -10 -20 -3 -1.5 0 1.5 3 H 40 0 80 120160200 probability of trials 0 0.15 0.3 0.45 72ms HTL n=6504 time after variance shift (ms) c f e 40 80 120160 200 probability of trials 54ms LTH n=6066 0 time after variance shift (ms) 0 0.15 0.3 0.45 Probability of trials 0 0.2 0.4 0.6 44ms LTH n=13623 time after variance shift (ms) 40 80 120160 200 0 n=13744 probability of trials 0 0.2 0.4 0.6 61ms HTL time after variance shift (ms) 40 80 120160 200 0 6. Variance shift detection on single trials: MT neuron pursuit LTH HTL b 0 100 150 200 threshold 50 trials time after variance shift (ms) threshold 0 5 10 15 1. Introduction and Experiments: The theory of efficient coding is linked to the idea that neural systems maximize information relevant to behavioral performance that can influence survival. Observations of neural responses in many organisms have demonstrated a capacity for efficient coding, but the consequences for behavior have not been explored. In our work, we demonstrate for the first time that efficient coding applies to a neural system as a whole, improving the accuracy of the movements it generates, and not solely to individual sensory neurons. We have exploited the close connection between cortical motion estimates and smooth pursuit eye movements to demonstrate parallel adaptation effects in sensory neurons and movement behavior. We find that adaptation to motion variance optimizes the encoding of motion information by MT neurons, with a behavioral impact of optimizing information in pursuit eye movements, minimizing visual tracking errors, and thereby improving vision of moving objects. 7. Discussion: Funding: Alfred P. Sloan Foundation ; Whitehall Foundation ; Brain Research Foundation ; NEI EY023371 1. Barlow HB, 1961. 2. Osborne LC and Lisberger SG, 2009 3. Osborne LC et al., 2005. 4. Fairhall AL et al., 2001. 5. Brenner et al., 2000. 6 . Wark B et al., 2009. 7 . Wark B et al., 2007. 0 0.2 0.4 0.6 0.8 -0.9 -0.6 -0.3 0 I (bits) n=11 I mean (bits) velocity (deg/s) HTL firing rate (spikes/s) time (ms) 0 30 0 500 1000 1500 HTL hvel vvel 0 60 time (ms) 0 500 1000 1500 stimulus (deg) 200 0 0 1000 2000 3000 time (ms) 150 0 time (ms) 0 1000 2000 3000 dots on MT neuron recording eye tracking stimulus (deg) SD (deg) SD (deg) MT neuron pursuit b a 60 30 0 -30 -60 -100 0 100 200 300 400 L (SD 12°) H (SD 35°) direction (deg) rate (spikes/s) L H -20 -80 -40 0 40 80 eye dir (deg) -10 0 10 20 L (SD 5°) H (SD 15°) L H direction (deg) rate/mean 4 2 0 -2 -4 0 2 4 6 L(SD 12°) H(SD 35°) direction/SD c direction/SD -8 -4 eye dir/mean -4 -2 0 2 4 L(SD 5°) H(SD 15°) 0 4 8 d e f gain index norm index filtered norm filtered 0 0.2 0.4 0.6 g/<g> -0.5 0 0.5 1 -1 fraction 0 0.1 0.2 0.3 0.4 g/<g> -0.5 0 0.5 1 -1 gain index norm index filtered norm filtered fraction time (ms) 0 100 150 200 error (deg) 0 4 8 12 data no adapt min error 50 direction error (deg) -30 -15 0 probability 0 0.1 0.2 0.3 0.4 0.5 data no adapt min error 15 30 b c a 0 0.5 1.5 2 1 gain scale factor rms error (deg) 0 6 12 18 SD 1° 2.5° 10° 15° 20° 25° 30° 36° 40° 45° d e f 0 target SD (deg) 10 20 30 40 50 error (deg) 0 0.5 1 1.5 2 2.5 er ga 0 120 0 150 0 target SD (deg) 10 20 30 40 50 pursuit error (deg) no adapt model data min error er ga direction (deg) -30 -15 0 15 30 stimulus data no adapt time (ms) 0 100 150 200 50 4. Optimal gain for minimizing pursuit error: 5. Gain adaptation depends on experienced stimulus values: -60 -30 0 L T H -100 0 100 200 300 400 direction (deg) 30 60 firing rate (spikes/s) a c e gain (spikes/s deg) direction SD (deg) 10 20 30 40 0 25 50 L to T L to H f LTH 12 time (ms) -100 -50 0 50 100 direction (deg) -60 -30 0 30 60 probability direction (deg) H -60 60 20 -20 T b L direction (deg) -80 -40 0 eye direction (deg) -20 -10 0 10 20 40 80 L T H d 0.6 n=11 L to T L to H gain 0 0.2 0.4 normalized SD L H MT neuron pursuit Barlow’s hypothesis of efficient sensory coding: −60 −30 0 30 60 0 0.05 0.1 probability −60 −30 0 30 60 0 0.5 1 stimulus value (s) response (r) stimulus distribution high gain low gain threshold

Rapid gain adaptation optimizes pursuit accuracyosbornelab.uchicago.edu/publications/cosyne_2016_BL.pdf · by adaptive gain in MT neurons and pursuit. Rapid recovery of mutual information

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Page 1: Rapid gain adaptation optimizes pursuit accuracyosbornelab.uchicago.edu/publications/cosyne_2016_BL.pdf · by adaptive gain in MT neurons and pursuit. Rapid recovery of mutual information

B. Liu, M.V. Macellaio and L.C. Osborne Rapid gain adaptation optimizes pursuit accuracy

Department of Neurobiology, The University of Chicago, Chicago IL, USA

2. Rescaling of response gain with stimulus variance in MT neurons and pursuit:

In the natural world, the statistics of sensory stimuli fluctuate across a wide range. In theory, the brain could maximize information recovery if sensory neurons adaptively rescale their sensitivity to match their limited response bandwidth to the current range of inputs. Such adaptive coding has been observed in a variety of systems, but the premise that adaptation optimizes behavior has not been tested. Here we show that adaptation in cortical sensory neurons maximizes information about visual motion, and minimizes tracking errors in pursuit eye movements guided by that cortical activity. Thus efficient sensory coding is not simply an ideal standard but rather a compact description of real sensory computation that manifests in improved behavioral performance.

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n=230 0.5 1.5

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info

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ion

(bits

)

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info

mat

ion

(bits

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normalized stimulus10.50-0.5-1

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form

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MT (n=94)pursuit (n=7)0

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3. Mutual information: Maximize information

by adaptive gain in MT neurons and pursuit.

Rapid recovery of mutual information after step change in direction variance.

prob

abilit

y

d

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a

eye direction (deg)

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et d

irect

ion

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6. Variance shift detection on single trials:MT neuron

pursuitLTH HTL

b

0 100 150 200

thre

shol

d

50

trials

time after variance shift (ms)

threshold

0

5

10

15

1. Introduction and Experiments:

The theory of efficient coding is linked to the idea that neural systems maximize information relevant to behavioral performance that can influence survival. Observations of neural responses in many organisms have demonstrated a capacity for efficient coding, but the consequences for behavior have not been explored. In our work, we demonstrate for the first time that efficient coding applies to a neural system as a whole, improving the accuracy of the movements it generates, and not solely to individual sensory neurons. We have exploited the close connection between cortical motion estimates and smooth pursuit eye movements to demonstrate parallel adaptation effects in sensory neurons and movement behavior. We find that adaptation to motion variance optimizes the encoding of motion information by MT neurons, with a behavioral impact of optimizing information in pursuit eye movements, minimizing visual tracking errors, and thereby improving vision of moving objects.

7. Discussion:

Funding: Alfred P. Sloan Foundation ; Whitehall Foundation ; Brain Research Foundation ; NEI EY023371 1. Barlow HB, 1961. 2. Osborne LC and Lisberger SG, 2009 3. Osborne LC et al., 2005. 4. Fairhall AL et al., 2001. 5. Brenner et al., 2000. 6. Wark B et al., 2009. 7. Wark B et al., 2007.

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4. Optimal gain for minimizing pursuit error:

5. Gain adaptation depends on experienced stimulus values:

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