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Role of Bees’ Sleep in
Memory Processing
ENT- 891- Doctoral Seminar (0+1)
KARTHIKEYAN, S (2015 800503)
Ph.D., Scholar,
Agricultural Entomology,
TNAU, Coimbatore.
Introduction
2
OUTLINE
Bees’ sleep
Sleep and memory processing
Case studies
 Effects Sleep on olfactory memory
 Effects Sleep on navigation memory
 Effects Sleep on waggle dance
 Effects of context odour presentation in sleep
 Electrophysiology of Sleep and brain activity
Conclusions
3
4
Circadian Clock and Sleep
 Role of circadian clock in bees
 Anticipate day–night fluctuations
 Time visits to flowers
 Time compensation when
referring to the sun in dance
 Regulation of sleep
 Molecular characterization suggests the clock of the
bee is more similar to mammals
Rothschild and Bloch (2008)5
“‘Hard-eyed’ creatures and insects manifestly assume the
posture of sleep; but the sleep of all such creatures is
of brief duration, so that often it might well baffle one’s
observation to decide whether they sleep or not.”
Do bees sleep?
6
(Aristotle, On Sleep and Sleeplessness 350 BC)
Yes they do! It seems…….
 Honey bees are the first invertebrates for which a
sleep-like state was described (Kaiser, 1983)
 Characteristic posture
• Flex legs
• Bringing its head to the floor
• Antennae stop moving
• Hold each others legs as they sleep
 Reduced muscle tonus
 Elevated response threshold (Piéron, 1913)
 Sleep rebound after sleep deprivation (Sauer, 2004)7
Sleep stages in bees
IA-Immobile-active state FS- First sleep stage
SS-Second sleep stage TS-Third sleep stage
Rothschild and Bloch (2008)8
Sleep in Task- Based Castes (Age Polyethism)
Klein et al., (2008) 9
Bees’ Sleep Vs Mammalian Sleep
 Characteristic posture
 Reduced muscle tonus
 Elevated response
threshold
 Sleep rebound after sleep
deprivation
 Persistence throughout life
 Bees’ sleep+ SWS
and REM sleep
MammalianBee
10
Sleep Function
 Energy conservation
 Restoration at the cellular and network levels
 Maintenance of synaptic homeostasis
 Memory consolidation
Rothschild and Bloch(2008)
Research confirms, there is strong link between
learning, memory and sleep (Rasch and Born, 2013)
11
12
Storage
Memory process
Encoding
Consolidation
Retrieval
s
l
e
e
p
 New memories are labile
 Sleep period strengthens or modifies memory13
s
l
e
e
p
 Well documented for humans (Born et al., 2006)
 Mammals (Siegel, 2005; Capellini et al., 2009)
 Birds (Jackson et al., 2008)
Sleep in Memory Processing
14
15
Navigation Memory
16
Navigation Memory
• RFID was used to record flights and behavior
• RFID bees behaved normally
• Bees released to unknown site
• Then those bees reached hive are sleep deprived
• And released from same site
17
Menzel et al., (2012)
18
Sleep and Navigation Memory
 Bees transferred to an unknown release site
 Sleep deprived: ~50% reached hive
 Sleep group: 1st Release 58%, 2nd Release 83%
Menzel et al., (2012)
19
Sleep Duration and Navigation Task
 Bees slept longer during the night following forced
navigation tasks
 Not due to exhaustion
 Distance didn’t affect sleep time during night
Menzel et al., (2012)
20
Olfactory Memory
21
 Classical Conditioning (CC) / Pavlov’s CC
Over the period of time
US CS
Extinction Learning (EL)
Continuous CS without US
CC
 Unconditioned Stimulus (US)
 Conditioned Stimulus (CS)
Proboscis Extension
Response (PER)
No PER
Concepts of Learning
sucrose
sucrose
22
 Classical Conditioning (CC) / Pavlov’s CC
Over the period of time
US CS
Extinction Learning (EL)
Continuous CS without US
CC
 Unconditioned Stimulus (US)
 Conditioned Stimulus (CS) No PER
Concepts of Learning
sucrose
sucrose
23
Proboscis Extension
Response (PER)
Sleep deprivation affects extinction but
not acquisition memory in honeybees
• Sleep deprivation had no effect on retention scores
after odor acquisition
• Whereas, retention for extinction learning was
significantly reduced
• Hence, consolidation of extinction memory was
affected by sleep deprivation but not acquisition
memory
Hussaini et al., (2009)
24
Sleep and Olfactory Memory
Hussaini et al., (2009)
sucrose
25
Context Odour
Presentation during Sleep
26
Context Odour Presentation during Sleep
Enhances Memory
Zwaka et al., (2015 )
27
Presentation of the Context Odour in Deep Sleep
Improves Retention after Single-Trial Learning
Zwaka et al., (2015 )
28
Context Odour Vs Novel Odour
Zwaka et al., (2015 ) 29
Presentation of the Context Odor in Wake
Phases Does Not Improve Retention
Zwaka et al., (2015 )30
Sleepy bees dances
sloppy
31
Sleep deprivation impairs precision of
waggle dance
 Slept bees (n = 7)
 SD of dance angles (13.78 ± 0.91)
 Sleep deprived bees (n = 6)
 SD of dance angles (16.49 ± 0.98)
 One angle per bee per day
 Greater the SD of dance angles; lesser the directional precision
Klein et al., (2010)
32
Bees’ Sleep and
Brain Activity
33
Electrophysiology of Bees’ Sleep
• Neuronal activity recorded in brain regions including
the mushroom bodies
• Nocturnal resting periods - the overall spike activity
was markedly increased
• Periodical variations of spike rate were present when
no visible antennal movements occurred
• Rhythmic brain activity in sleeping bees
Schuppe, (2015 )
34
Conclusions
 Sleep has an absolute role in memory processing
 Honey bees an attractive model to study sleep,
memory and learning in a natural context
 Small brain (with about 1 million neurons)
 Smart learners
 Learning is reinforced during sleep – humans?
BEES’ MAGIC WELL IS NOWHERE NEAR EMPTY
35
References
Beyaert, L., Greggers, U., Menzel, R., 2012. Honeybees consolidate
navigation memory during sleep. J. Exp. Biol. 215, 3981–3988.
Eban-Rothschild, A.D., Bloch, G., 2008. Differences in the sleep
architecture of foragerand young honeybees (Apis mellifera). J.
Exp. Biol. 211, 2408–2416.
Hussaini, S.A., Bogusch, L., Landgraf, T., Menzel, R., 2009. Sleep
deprivation affects extinction but not acquisition memory in
honeybees. Learn. Mem. 16, 698–705.
Menzel, R., 2012. The honeybee as a model for understanding the basis of
cognition. Nat. Rev. Neurosci. 13, 758–768.
Klein BA, Olzsowy KM, Klein A, Saunders KM, Seeley TD (2008) Caste-
dependent sleep of worker honey bees. J Exp Biol. 211:3028– 3040.
Eban-Rothschild, A. D., Bloch, G. (2012) Circadian Rhythms and Sleep in
Honey Bees, chapter 1.3., p. 31-46 in “Honeybee Neurobiology
and Behavior: A Tribute to Randolf Menzel”.
Kaiser, W. 1988 Busy bees need rest, too-behavioural and electromyographical
sleep signs in honeybees, J. Comp. Physiol. 163: 565–584. 36

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Role of bees’ sleep in memory processing

  • 1. Role of Bees’ Sleep in Memory Processing ENT- 891- Doctoral Seminar (0+1) KARTHIKEYAN, S (2015 800503) Ph.D., Scholar, Agricultural Entomology, TNAU, Coimbatore.
  • 3. OUTLINE Bees’ sleep Sleep and memory processing Case studies  Effects Sleep on olfactory memory  Effects Sleep on navigation memory  Effects Sleep on waggle dance  Effects of context odour presentation in sleep  Electrophysiology of Sleep and brain activity Conclusions 3
  • 4. 4
  • 5. Circadian Clock and Sleep  Role of circadian clock in bees  Anticipate day–night fluctuations  Time visits to flowers  Time compensation when referring to the sun in dance  Regulation of sleep  Molecular characterization suggests the clock of the bee is more similar to mammals Rothschild and Bloch (2008)5
  • 6. “‘Hard-eyed’ creatures and insects manifestly assume the posture of sleep; but the sleep of all such creatures is of brief duration, so that often it might well baffle one’s observation to decide whether they sleep or not.” Do bees sleep? 6 (Aristotle, On Sleep and Sleeplessness 350 BC)
  • 7. Yes they do! It seems…….  Honey bees are the first invertebrates for which a sleep-like state was described (Kaiser, 1983)  Characteristic posture • Flex legs • Bringing its head to the floor • Antennae stop moving • Hold each others legs as they sleep  Reduced muscle tonus  Elevated response threshold (Piéron, 1913)  Sleep rebound after sleep deprivation (Sauer, 2004)7
  • 8. Sleep stages in bees IA-Immobile-active state FS- First sleep stage SS-Second sleep stage TS-Third sleep stage Rothschild and Bloch (2008)8
  • 9. Sleep in Task- Based Castes (Age Polyethism) Klein et al., (2008) 9
  • 10. Bees’ Sleep Vs Mammalian Sleep  Characteristic posture  Reduced muscle tonus  Elevated response threshold  Sleep rebound after sleep deprivation  Persistence throughout life  Bees’ sleep+ SWS and REM sleep MammalianBee 10
  • 11. Sleep Function  Energy conservation  Restoration at the cellular and network levels  Maintenance of synaptic homeostasis  Memory consolidation Rothschild and Bloch(2008) Research confirms, there is strong link between learning, memory and sleep (Rasch and Born, 2013) 11
  • 12. 12
  • 13. Storage Memory process Encoding Consolidation Retrieval s l e e p  New memories are labile  Sleep period strengthens or modifies memory13 s l e e p
  • 14.  Well documented for humans (Born et al., 2006)  Mammals (Siegel, 2005; Capellini et al., 2009)  Birds (Jackson et al., 2008) Sleep in Memory Processing 14
  • 15. 15
  • 17. Navigation Memory • RFID was used to record flights and behavior • RFID bees behaved normally • Bees released to unknown site • Then those bees reached hive are sleep deprived • And released from same site 17
  • 18. Menzel et al., (2012) 18
  • 19. Sleep and Navigation Memory  Bees transferred to an unknown release site  Sleep deprived: ~50% reached hive  Sleep group: 1st Release 58%, 2nd Release 83% Menzel et al., (2012) 19
  • 20. Sleep Duration and Navigation Task  Bees slept longer during the night following forced navigation tasks  Not due to exhaustion  Distance didn’t affect sleep time during night Menzel et al., (2012) 20
  • 22.  Classical Conditioning (CC) / Pavlov’s CC Over the period of time US CS Extinction Learning (EL) Continuous CS without US CC  Unconditioned Stimulus (US)  Conditioned Stimulus (CS) Proboscis Extension Response (PER) No PER Concepts of Learning sucrose sucrose 22
  • 23.  Classical Conditioning (CC) / Pavlov’s CC Over the period of time US CS Extinction Learning (EL) Continuous CS without US CC  Unconditioned Stimulus (US)  Conditioned Stimulus (CS) No PER Concepts of Learning sucrose sucrose 23 Proboscis Extension Response (PER)
  • 24. Sleep deprivation affects extinction but not acquisition memory in honeybees • Sleep deprivation had no effect on retention scores after odor acquisition • Whereas, retention for extinction learning was significantly reduced • Hence, consolidation of extinction memory was affected by sleep deprivation but not acquisition memory Hussaini et al., (2009) 24
  • 25. Sleep and Olfactory Memory Hussaini et al., (2009) sucrose 25
  • 27. Context Odour Presentation during Sleep Enhances Memory Zwaka et al., (2015 ) 27
  • 28. Presentation of the Context Odour in Deep Sleep Improves Retention after Single-Trial Learning Zwaka et al., (2015 ) 28
  • 29. Context Odour Vs Novel Odour Zwaka et al., (2015 ) 29
  • 30. Presentation of the Context Odor in Wake Phases Does Not Improve Retention Zwaka et al., (2015 )30
  • 32. Sleep deprivation impairs precision of waggle dance  Slept bees (n = 7)  SD of dance angles (13.78 ± 0.91)  Sleep deprived bees (n = 6)  SD of dance angles (16.49 ± 0.98)  One angle per bee per day  Greater the SD of dance angles; lesser the directional precision Klein et al., (2010) 32
  • 33. Bees’ Sleep and Brain Activity 33
  • 34. Electrophysiology of Bees’ Sleep • Neuronal activity recorded in brain regions including the mushroom bodies • Nocturnal resting periods - the overall spike activity was markedly increased • Periodical variations of spike rate were present when no visible antennal movements occurred • Rhythmic brain activity in sleeping bees Schuppe, (2015 ) 34
  • 35. Conclusions  Sleep has an absolute role in memory processing  Honey bees an attractive model to study sleep, memory and learning in a natural context  Small brain (with about 1 million neurons)  Smart learners  Learning is reinforced during sleep – humans? BEES’ MAGIC WELL IS NOWHERE NEAR EMPTY 35
  • 36. References Beyaert, L., Greggers, U., Menzel, R., 2012. Honeybees consolidate navigation memory during sleep. J. Exp. Biol. 215, 3981–3988. Eban-Rothschild, A.D., Bloch, G., 2008. Differences in the sleep architecture of foragerand young honeybees (Apis mellifera). J. Exp. Biol. 211, 2408–2416. Hussaini, S.A., Bogusch, L., Landgraf, T., Menzel, R., 2009. Sleep deprivation affects extinction but not acquisition memory in honeybees. Learn. Mem. 16, 698–705. Menzel, R., 2012. The honeybee as a model for understanding the basis of cognition. Nat. Rev. Neurosci. 13, 758–768. Klein BA, Olzsowy KM, Klein A, Saunders KM, Seeley TD (2008) Caste- dependent sleep of worker honey bees. J Exp Biol. 211:3028– 3040. Eban-Rothschild, A. D., Bloch, G. (2012) Circadian Rhythms and Sleep in Honey Bees, chapter 1.3., p. 31-46 in “Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel”. Kaiser, W. 1988 Busy bees need rest, too-behavioural and electromyographical sleep signs in honeybees, J. Comp. Physiol. 163: 565–584. 36

Editor's Notes

  1. Elevated response threshold-higher intensity stimulus is needed to produce a response
  2. [IA] – an awake bee stays in the same place, the thorax, abdomen, and head are clearly raised above the substrate. [FS] – the abdomen and thorax are clearly raised above the substrate, and the antennae are extended at an angle of 90–180°, between the pedicle and the scape. [SS] – body is typically more adjacent to the substrate, and the antennae are extended at an angle of ~90° between the pedicle and the scape. [TS] – the muscle tonus is reduced, and the body is adjacent to the substrate. The angle between the pedicle and scape < 90°, with the antennae tips typically touching the substrate.
  3. 3 days as a cell cleaner, 4–12 of as a ‘nurse bee’, 13–20 as a ‘food storer’
  4. (I) Encoding - up-take of the information to be stored into a neural representation. (II) Consolidation - stabilization of the memory that follows encoding and enables the retention of a memory over time. In the absence of such consolidation the information would be rapidly forgotten. Forgetting can result from a decay of the memory trace or from retroactive interference as the encoding of new information leads to an overwriting of the information encoded before. (III) Retrieval of the stored information refers to the reactivation of a stored memory in the context of more or less goal-directed behavior.
  5. IMM-intermediate and medial mesopallium, unknown locus termed S
  6. The bee in A was trained to a feeder close to the hive (distance 10m), The two bees in B and C were trained to a feeder 200m east of the hive. The small triangles indicate colored tents serving as radartransparent landmarks