Virtually all sensory experience occurs in the context of active behaviors

1 2

3 4 5

• In many cases, sensing actions are central to the task of collecting accurate information about the environment.

• Sensing actions involve moving the stimulus object with respect to the sense organ, or perturbing the stimulus object in some way.

Thesis: sensing and “sensing actions” are processed in a concerted fashion

• Knowledge of sensing actions can be critical to the interpretation of sensory signals.

http://webvision.med.utah.edu

Specializations of the retinal fovea: densest packing of photoreceptors and lowest convergence of

photoreceptors onto ganglion cells

http://webvision.med.utah.edu

Specializations of the retinal fovea: displacement of inner retina

http://webvision.med.utah.edu

Specializations of the retinal fovea: absence of retinal vasculature

Hans-Werner Hunziker, (2006) “Im Auge des Lesers”, Transmedia Stäubli Verlag Zürich

Acute vision only occurs within a few degrees of the fovea

Saccadic eye movements bring objects into the fovea

We make a saccade 2-3 times per second.

The problem with eye movements #1:

Solution: the visual system interprets visual signals in the context of knowledge about coordinated eye movements.

Problem: eye movements create fictive motion of the image on the retina.

-- Hermann von Helmholtz, Physiologische Optiktrans. William James, The Principles of Psychology

The problem with eye movements #2:

Solution: visual signals are suppressed during saccades.

Problem: eye movements blur the image on the retina.

cat LGN, spontaneous saccades in the dark, avg of 71 cells Lee & Malpeli, J. Neurophysiol. 1998

The problem with eye movements #3:

Stein & Stanford 2008

Solution: eye position modifies the auditory receptive fields of superior colliculus neurons.

Problem: eye movements change the relationship between the visual world and the head, so visual and auditory maps are misaligned.

The problem with head movements:

Boyden, Katoh, & Raymond Annu. Rev. Neurosci. 2004

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.

Problem: head movements cause a stationary object to move out of the fovea.

Sabin, Macpherson , & Middlebrooks, Hearing Res. 2004 human psychophysics

Hearing: localization acuity depends on source position

Thus, head movements can “foveate” an auditory stimulus.

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.

Hedwig & Poulet Science 2006

CDI morphology:

Olfaction: sniffing is an active process

Kepecs, Uchida, & Mainen J. Neurophysiol. 2007

Novel odors can trigger rapid increases in sniff rate

rat Wesson et al., PloS Biology 2008

2-alternative forced-choice w/ water reward Uchida & Mainen, Nat. Neurosci. 2003

A two-alternative forced-choice paradigm for odor discrimination

Wesson et al., Chem. Senses 2008

Sniff rate increases in anticipation of an odor

mouse 1

mouse 2

mouse 3

2-alternative forced-choice w/ water reward

Rapid sniffing attenuates olfactory receptor neuron inputto the olfactory bulb

head-fixed rat, rat calcium imaging w/ OGB Verhagen et al., Nat. Neurosci. 2007

Verhagen et al., Nat. Neurosci. 2007

Effects of rapid sniffing are bottom-up (not top-down)

head-fixed rat, rat calcium imaging w/ OGB

Kleinfeld, Ahissar, & Diamond, Curr. Opin. Neurobiol. 2006Adapted from Fee, Mitra, & Kleinfeld, J. Neurophysiol. 1997

Somatosensation: rodent whisking as a model for active encounters with somatosensory stimuli

The whisker pad has a large representation in the somatosensory cortex of the rodent

Petersen Pflugers Arch. 2003

Somatosensory cortex contains “reference signals” about whisker motion

Crochet & Petersen, Nat. Neurosci. 2006whole-cell patch-clamp recording from awake mouse

Responses to whisker deflection in barrel cortexdepend on whether the animal is actively whisking

Ferezou, Petersen et al, Neuron 2006

Kleinfeld, Ahissar, & Diamond, Curr. Opin. Neurobiol. 2006

Somatosensory and motor circuits are linked by sensorimotor loops

1°

2°

3°

4°

motor neurons

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Electrosensation: sensory exotica

Gnathonemus petersii

see e.g., Sensory Exotica: A World beyond Human Experience, by H. Hughes (MIT Press, 2001)

electric organ discharge command nucleus

electric organ electrosensory receptor neurons

electric organ discharge

(EOD)

fish

water

adapted from Bell J. Exp. Biol. 1989

electrosensory lobe(ELL)

higher brain regions

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.

Active sensing in electrosensation

electric organ discharge command nucleus

electric organ electrosensory receptor neurons

electric organ discharge

(EOD)

electric organ corollary discharge

(EOCD)

fish

water

adapted from Bell J. Exp. Biol. 1989

electrosensory lobe(ELL)

higher brain regions

intramuscularcurare

local lidocaine

metalliccurrent sink

EOD command (effect on the electric organ is blocked with curare)

command alone

command alone

command + electrosensory stimulus 1.5 msec later

80 msec

(9 min)

Bell Brain Res. 1986

Plastic responses to corollary discharge

1 min

recording from mormyrid ELL

electric organ discharge command nucleus

electric organ electrosensory receptor neurons

electric organ discharge

(EOD)

electric organ corollary discharge

(EOCD)

fish

water

adapted from Bell J. Exp. Biol. 1989

proprioceptors

electrosensory lobe(ELL)

higher brain regions

Bastien J. Comp. Physiol. 1995

Plastic responses to proprioceptive stimuli

recording from gymnotid ELL