Complex inter and intraregional oscillatory dynamics in olfactory processing

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Complex inter- and intraregional oscillatory
dynamics inolfactory processing

• Leslie M. Kay
• Department of Psychology
• The University of Chicago

U Chicago Boston University Jennifer Beshel Nancy
Kopell Claire Martin Jorge Brea Catherine
Lowry Ehud Sivan
Funding NIDCD (CRCNS) and Brain Research
Foundation
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Olfactory System Feed-Forward
Olfactory Bulb Input
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Olfactory bulb architectureand chemotopic
representation
Johnson et al., J Comp Neurol, 2005
Adapted from Shepherd, The Synaptic Organization
of the Brain
Adapted from Mori et al., J Neurophys 1992
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Chemotopic Representation and Odor Similarity

• Mice generalize to similar aliphatic compounds.
• also Linster Hasselmo, 1999 (rats), Laska et
  al., 1999 (humans squirrel monkeys)

Digging (Z-score)
Chain length difference
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Single neuron and population measures
1-300 Hz
600Hz-9KHz
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Olfactory Bulb
/-

JG
JG
ORN
/-

MC

-

MC
GC


-
-
-

GC
-

Input from other olfactory and limbic areas
Piriform Cortex
MC mitral cells GC granule cells ORN
olfactory receptor neurons JG juxtaglomeruluar
cells
Fig. adapted from Freeman, 1975
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Olfactory Bulb Slow OscillationsRespiration and
OB theta rhythm
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Mitral cells slow temporal firing patterns
follow the respiratory/theta rhythm
Except During fast sniffing (gt5 Hz)
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Olfactory Bulb Fast Oscillations
Sniffs (theta 2-12 Hz)
gamma bursts 70 Hz
Kay, J Integ Neurosci, 2003
Lowry Kay, J Neurophys 2007
Martin et al., in review
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Mitral cells fine temporal firing patterns
follow the gamma oscillation
0.25 second

-

mitral cells
granule cells
Eeckman Freeman, Brain Research 1990
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Fast sniffing and disrupted olfactory bulb gamma
oscillations
Mitral cells also change from burst to tonic
firing mode
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Mechanisms Regulating PrecisionCentrifugal
input to the OB
MC mitral cells GC granule cells ORN
olfactory receptor neurons JG juxtaglomeruluar
cells
Gray Skinner, Exp Brain Res 1988 Martin et al.,
Eur J Neurosci 2006
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Mechanisms regulating precision Inhibition in
the honeybee antennal lobe
ORN

PN

-

PN
LN

-
-
-

LN
-

Input from anterior olfactory nucleus
Input from other olfactory and limbic areas
MacLeod Laurent, Science 1996 Stopfer et al.,
Nature 1997
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Mechanisms Regulating Precision Inhibition of
GABAergic cells
/-

JG
ORN
JG

/-

MC

-


MC
GC
-
-
-

GC
-
MC mitral cells GC granule cells ORN
olfactory receptor neurons JG juxtaglomeruluar
cells

Input from anterior olfactory nucleus
Input from other olfactory and limbic areas
Nusser et al., J Neurophys 2001
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Enhanced gamma and decreased odor generalization
in ß3-/- mice
2 seconds
Nusser et al., J Neurophys 2001 Kay, J Integ
Neurosci 2003
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Is this functional?

• Can an animal adjust the level of synchrony
  online?

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Fine vs. Coarse Odor Discrimination
OH
OH
butanol
hexanol
OH
OH
octanol
heptanol
hexanol
heptanol

• Hypothesis
• Fine discrimination tasks require synchrony and
  should show larger gamma power

Beshel, Kopell Kay, in review
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Context modulates synchrony
coarse
gamma filtered data
fine
Beshel, Kopell Kay, in review
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The coarse task may use a feed-forward system

• Enhanced evoked potential
• Enhanced gamma appears the same as in the case of
  the isolated bulb

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However
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Learning-associated beta oscillations Go /
No-Go task
OB - dHPC
OB - vHPC
dHPC - vHPC
Strongly coherent with the PC Requires input from
PC Predicts onset of criterion behavior Martin
et al., J Neurosci 2004
Martin, Beshel Kay, in review
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Odor-induced beta oscillations sensitization
Trial 1
Trial 11
Lowry Kay, J Neurophys 2007
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Beta power and odorant volatility
High volatility 1-120 mm Hg
Low volatility lt 1 mm Hg
mixtures
gt 120 mm Hg
Lowry Kay, J Neurophys 2007
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Theta band (respiratory) OB-PC coherence scales
with volatility
anesthetized
waking
Lowry Kay, J Neurophys 2007
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Odor-evoked beta oscillation dynamical context
Do learning induced beta oscillations present a
similar profile?
Lowry Kay, J Neurophys 2007
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Olfactory Bulb
/-

JG
JG
ORN
/-

MC

-

MC
GC


-
-
-

GC
-

Input from other olfactory and limbic areas
Piriform Cortex
MC mitral cells GC granule cells ORN
olfactory receptor neurons JG juxtaglomeruluar
cells
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Connections with other systemsolfactory-hippocam
pal connections and the limbic respiratory loop
HPC
EC
temp HPC
PC
OB- olfactory bulb PC- piriform cortex EC-
entorhinal cortex HPC- hippocampus
OB
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Olfactory Bulb / Hippocampus Theta Rhythms
Odor begins
Kay PNAS 2005
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OB-HPC theta coherence is correlated with
performance
Olfactory bulb and hippocampus can lock at
sniffing frequency during odor sniffing (high
theta 7-12 Hz) Magnitude of locking is strongly
correlated with performance
Kay PNAS 2005
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Dynamics span several time scales
Kay, Chaos, 2003
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Conclusions

• Fast oscillations in OB are associated with
  pattern discrimination difficulty
• The level and type of fast oscillatory synchrony
  is modulated according to task demands
• Overall system connectivity and dynamical
  structure is dependent on context / task

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Behavioral effects of airborne concentration
Lowry Kay, J Neurophys 2007