Lecture 12: olfaction: the insect antennal lobe

References:H C Mulvad, thesis (http://www.nordita.dk/~mulvad/Thesis), Ch 2G Laurent, Trends Neurosci 19 489-496 (1996)M Bazhenov et al, Neuron 30 553-567 and 569-581 (2001)Dayan & Abbott, Sect 7.5

Olfaction (smell)

Olfaction (smell)The oldest sense (even bacteria do it)

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Basic anatomy:

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Basic anatomy:Insects: receptor cells -> antennal lobe -> mushroom bodies

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Basic anatomy:Insects: receptor cells -> antennal lobe -> mushroom bodiesMammals: receptor cells -> olfactory bulb -> olfactory cortex

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Basic anatomy:Insects: receptor cells -> antennal lobe -> mushroom bodiesMammals: receptor cells -> olfactory bulb -> olfactory cortex

~100000 receptor cells, several hundred types (distinguished by receptor proteins)

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Basic anatomy:Insects: receptor cells -> antennal lobe -> mushroom bodiesMammals: receptor cells -> olfactory bulb -> olfactory cortex

~100000 receptor cells, several hundred types (distinguished by receptor proteins)any cell responsive to a range of odorants:

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Basic anatomy:Insects: receptor cells -> antennal lobe -> mushroom bodiesMammals: receptor cells -> olfactory bulb -> olfactory cortex

~100000 receptor cells, several hundred types (distinguished by receptor proteins)any cell responsive to a range of odorants: => an odor produces a characteristic pattern of activity

across the receptor cell population

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Basic anatomy:Insects: receptor cells -> antennal lobe -> mushroom bodiesMammals: receptor cells -> olfactory bulb -> olfactory cortex

~100000 receptor cells, several hundred types (distinguished by receptor proteins)any cell responsive to a range of odorants: => an odor produces a characteristic pattern of activity

across the receptor cell population

Receptor physiology: Receptor proteins (1 kind/cell): metabotropic, G-protein coupled,

lead to opening of Na channels

Olfaction (smell)The oldest sense (even bacteria do it)

Highly conserved in evolution (mammals and insects similar)

Basic anatomy:Insects: receptor cells -> antennal lobe -> mushroom bodiesMammals: receptor cells -> olfactory bulb -> olfactory cortex

~100000 receptor cells, several hundred types (distinguished by receptor proteins)any cell responsive to a range of odorants: => an odor produces a characteristic pattern of activity

across the receptor cell population

Receptor physiology: Receptor proteins (1 kind/cell): metabotropic, G-protein coupled,

lead to opening of Na channels, similar to phototransductionin retina

Antennal lobe~1000-10000 neurons

in locust: 1130: 830 excitatory, 300 inhibitoryin honeybee: 800 excitatory, 4000 inhibitory

Antennal lobe~1000-10000 neurons

in locust: 1130: 830 excitatory, 300 inhibitoryin honeybee: 800 excitatory, 4000 inhibitory

Organized into glomeruli (bunches of synapes) (~1000 in locust, 160 in bee)

Antennal lobe~1000-10000 neurons

in locust: 1130: 830 excitatory, 300 inhibitoryin honeybee: 800 excitatory, 4000 inhibitory

Organized into glomeruli (bunches of synapes) (~1000 in locust, 160 in bee)

Antennal lobe~1000-10000 neurons

in locust: 1130: 830 excitatory, 300 inhibitoryin honeybee: 800 excitatory, 4000 inhibitory

Organized into glomeruli (bunches of synapes) (~1000 in locust, 160 in bee)

Connections between ALneurons: dendrodentritic

Excitatory cells (PN)PN = projection neuron: axon takes its spikes out of the antennal

lobe, to the mushroom bodies (+ other higher areas)

Excitatory cells (PN)PN = projection neuron: axon takes its spikes out of the antennal

lobe, to the mushroom bodies (+ other higher areas) transmitter: ACh

Excitatory cells (PN)PN = projection neuron: axon takes its spikes out of the antennal

lobe, to the mushroom bodies (+ other higher areas) transmitter: ACh

Excitatory cells (PN)PN = projection neuron: axon takes its spikes out of the antennal

lobe, to the mushroom bodies (+ other higher areas) transmitter: ACh

Dendrites have postsynaptic terminalsin 1 or more glomeruli

(10-20 in locust)

Inhibitory cells (LN)LN = local neuron: projects only within the antennal lobe

Inhibitory cells (LN)LN = local neuron: projects only within the antennal lobe

no Na spikes, only Ca “spikelets”

Inhibitory cells (LN)LN = local neuron: projects only within the antennal lobe

no Na spikes, only Ca “spikelets”transmitter: GABA

Inhibitory cells (LN)LN = local neuron: projects only within the antennal lobe

no Na spikes, only Ca “spikelets”transmitter: GABA

Inhibitory cells (LN)LN = local neuron: projects only within the antennal lobe

no Na spikes, only Ca “spikelets”transmitter: GABA

Dendrites with postsynaptic terminals in several or all glomeruli

Antennal lobe responses:temporally modulated oscillatory activity patterns

Antennal lobe responses:temporally modulated oscillatory activity patterns

~20 hz oscillations:

Antennal lobe responses:temporally modulated oscillatory activity patterns

(No oscillations in input from receptor cells)

~20 hz oscillations:

Oscillations and transient synchronization

membrane potentials

Oscillations and transient synchronization

membrane potentials

Local field potentialIn mushroom body:Measures averageAL activity

(cell in mushroom body)

Oscillations and transient synchronization

membrane potentials

Local field potentialIn mushroom body:Measures averageAL activity

PN firing transientlysynchronized toLFP

(cell in mushroom body)

Model (Bazhenov et al)

• 90 PNs, 30 LNs

Model (Bazhenov et al)

•90 PNs, 30 LNs

•Single-compartment, conductance-based neurons

Model (Bazhenov et al)

•90 PNs, 30 LNs

•Single-compartment, conductance-based neurons

•(post)synaptic kinetics

Model (Bazhenov et al)

•90 PNs, 30 LNs

•Single-compartment, conductance-based neurons

•(post)synaptic kinetics

•Fast excitation, fast and slow inhibition

Model (Bazhenov et al)

•90 PNs, 30 LNs

•Single-compartment, conductance-based neurons

•(post)synaptic kinetics

•Fast excitation, fast and slow inhibition

•50% connectivity, random

Model (Bazhenov et al)

•90 PNs, 30 LNs

•Single-compartment, conductance-based neurons

•(post)synaptic kinetics

•Fast excitation, fast and slow inhibition

•50% connectivity, random

•Stimuli: 1-s current pulse inputs to randomly-chosen 33% of neurons

Bazhenov network

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

Active currents:

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

)(3NaNaNa VVhmgI

Active currents:Na

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

)(3NaNaNa VVhmgI )(4 KKK VVngI

Active currents:Na K

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

)(3NaNaNa VVhmgI )(4 KKK VVngI )(4

KAAAA VVhmgI

Active currents:Na K A-current

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

)(3NaNaNa VVhmgI )(4 KKK VVngI )(4

KAAAA VVhmgI

inhslowGABAnAChsyn IIIIA

Active currents:Na K A-current

Synaptic input

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

)(3NaNaNa VVhmgI )(4 KKK VVngI )(4

KAAAA VVhmgI

inhslowGABAnAChsyn IIIIA

)]([ ssfast VVOgI

Active currents:Na K A-current

Synaptic input

Fast (ionotropic) synaptic currents (nACh and GABAA):

( [O] is open fraction)

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

)(3NaNaNa VVhmgI )(4 KKK VVngI )(4

KAAAA VVhmgI

inhslowGABAnAChsyn IIIIA

)]([ ssfast VVOgI ][]])[[1(][

OTOdtOd

Active currents:Na K A-current

Synaptic input

Fast (ionotropic) synaptic currents (nACh and GABAA):

( [O] is open fraction)

[T] is transmitter concentration:

Excitatory neurons

stimsynAKNaLL IIIIIVVgdtdV

C )(

)(3NaNaNa VVhmgI )(4 KKK VVngI )(4

KAAAA VVhmgI

inhslowGABAnAChsyn IIIIA

)]([ ssfast VVOgI ][]])[[1(][

OTOdtOd

]/))((exp[11

][

)()(][

0

0max0

VtVT

tttttAT

Active currents:Na K A-current

Synaptic input

Fast (ionotropic) synaptic currents (nACh and GABAA):

( [O] is open fraction)

[T] is transmitter concentration: exc

inh

Slow inhibition

Kinetics like GABAB )(][][

4

4

Kslowinhslow VVKG

GgI

Slow inhibition

Kinetics like GABAB )(][][

4

4

Kslowinhslow VVKG

GgI

][][][

43 GrRrdtGd G-protein concentration:

Slow inhibition

Kinetics like GABAB )(][][

4

4

Kslowinhslow VVKG

GgI

][][][

43 GrRrdtGd

][]])[[1(][

21 RrTRrdtRd

G-protein concentration:

Activated receptor concentration

Slow inhibition

Kinetics like GABAB )(][][

4

4

Kslowinhslow VVKG

GgI

][][][

43 GrRrdtGd

][]])[[1(][

21 RrTRrdtRd

G-protein concentration:

Activated receptor concentration

Fast and slowComponents:

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

Active currents:

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

)(2CaCaCaCaCa VVhmgI

Active currents:Ca

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

)(2CaCaCaCaCa VVhmgI

Active currents:Ca

( -> Ca spikes)

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

)(2CaCaCaCaCa VVhmgI )(4 KKK VVngI

Active currents:Ca K

( -> Ca spikes)

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

)(2CaCaCaCaCa VVhmgI )(4 KKK VVngI )()()()( KCaKCaKCaK VVngI

Active currents:Ca K Ca-dependent K current

( -> Ca spikes)

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

)(2CaCaCaCaCa VVhmgI )(4 KKK VVngI )()()()( KCaKCaKCaK VVngI

Active currents:Ca K Ca-dependent K current

( -> spike rate adaptation)( -> Ca spikes)

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

)(2CaCaCaCaCa VVhmgI )(4 KKK VVngI )()()()( KCaKCaKCaK VVngI

2][100

,2][][ )()(

CaCa

Can CaK

nCaK

Active currents:Ca K Ca-dependent K current

Dynamics of nK(Ca):

( -> spike rate adaptation)( -> Ca spikes)

Inhibitory neurons

stimsynCaKKCaLL IIIIIVVgdtdV

C )()(

)(2CaCaCaCaCa VVhmgI )(4 KKK VVngI )()()()( KCaKCaKCaK VVngI

)][]([][ CaCa

IdtCad

Ca

2][100

,2][][ )()(

CaCa

Can CaK

nCaK

Active currents:Ca K Ca-dependent K current

Dynamics of nK(Ca):

Ca dynamics:

( -> spike rate adaptation)( -> Ca spikes)

2 neurons (1 PN, 1LN)

6 PNs + 2 LNs

6 PNs + 2 LNs(fast) inhibition between LNs

6 PNs + 2 LNs(fast) inhibition between LNs

6 PNs + 2 LNs(fast) inhibition between LNs

LNs take turns:

Full network (90+30)

Responses of 4 PNs to 1 stimulus

Responses of 4 PNs to 1 stimulus

Reliable (trial-to-trial reproducible) firing timing when there is largeInhibitory input

Another stimulus:Input to same set of PNs but different LNs

Another stimulus:Input to same set of PNs but different LNs

Another stimulus:Input to same set of PNs but different LNs

Same overall firing rate pattern, but different temporal fine structure

3rd stimulus:Input to 90%-different set of neurons:

3rd stimulus:Input to 90%-different set of neurons:

3rd stimulus:Input to 90%-different set of neurons:

Different firing pattern across neurons (but same network-average rate)

Blocking LN-LN inhibitionLNs now spike ~ regularly

Blocking LN-LN inhibitionLNs now spike ~ regularly

Less difference between responses to stimuli 1 and 2

Reducing IK(Ca) (reducing LN spike-rate adaptation)

Reducing IK(Ca) (reducing LN spike-rate adaptation)

Reducing IK(Ca)

Less precise timing, weaker temporal modulation, reduced discriminability

(reducing LN spike-rate adaptation)

Role of slow LN-PN inhibition

Role of slow LN-PN inhibition

Slow rate modulationsabolished

Role of slow LN-PN inhibition

Slow rate modulationsabolished

reduced discriminability