Virtually all sensory experience
occurs in the context of active behaviors
1
3
2
4
5
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.
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
http://webvision.med.utah.edu
Acute vision only occurs within a few degrees of the fovea
Hans-Werner Hunziker, (2006) “Im Auge des Lesers”, Transmedia Stäubli Verlag Zürich
Saccadic eye movements bring objects into the fovea
We make a saccade 2-3 times per second.
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
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
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
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
Hearing: localization acuity depends on source position
Thus, head movements can “foveate” an auditory stimulus.
human psychophysics
Sabin, Macpherson , & Middlebrooks, Hearing Res. 2004
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
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
A two-alternative forced-choice paradigm
for odor discrimination
2-alternative forced-choice w/ water reward
Uchida & Mainen, Nat. Neurosci. 2003
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
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
Effects of rapid sniffing are bottom-up (not top-down)
head-fixed rat, rat calcium imaging w/ OGB
Verhagen et al., Nat. Neurosci. 2007
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
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
whole-cell patch-clamp recording from awake mouse
Crochet & Petersen, Nat. Neurosci. 2006
Responses to whisker deflection in barrel cortex
depend on whether the animal is actively whisking
Ferezou, Petersen et al, Neuron 2006
Somatosensory and motor circuits
are linked by sensorimotor loops
4°
extralemniscal (touch)
3°
2°
motor
neurons
1°
Kleinfeld, Ahissar, & Diamond, Curr. Opin. Neurobiol. 2006
Electrosensation: sensory exotica
Gnathonemus petersii
see e.g., Sensory Exotica: A World beyond Human Experience, by H. Hughes (MIT Press, 2001)
Active sensing in electrosensation
higher brain regions
electric organ discharge
command nucleus
electric organ
electrosensory lobe
(ELL)
electrosensory receptor neurons
fish
water
electric organ
discharge
(EOD)
adapted from Bell J. Exp. Biol. 1989
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.
higher brain regions
local lidocaine
electric organ discharge
command nucleus
electric organ
corollary discharge
(EOCD)
electrosensory lobe
(ELL)
intramuscular
curare
electric organ
electrosensory receptor neurons
fish
water
metallic
current sink
electric organ
discharge
(EOD)
adapted from Bell J. Exp. Biol. 1989
Plastic responses to corollary discharge
EOD command (effect on the electric organ is blocked with curare)
command alone
(9 min)
command
+ electrosensory stimulus 1.5 msec later
command alone
1 min
recording from mormyrid ELL
80 msec
Bell Brain Res. 1986
higher brain regions
electric organ discharge
command nucleus
electric organ
electric organ
corollary discharge
(EOCD)
electrosensory lobe
(ELL)
electrosensory receptor neurons
proprioceptors
fish
water
electric organ
discharge
(EOD)
adapted from Bell J. Exp. Biol. 1989
Plastic responses to proprioceptive stimuli
recording from gymnotid ELL
Bastien J. Comp. Physiol. 1995