LABORATORY OF NEUROBIOLOGY
AND BEHAVIOR
Head:
Prof.
Abraham J. Susswein
Department
of Life Sciences, Bar-Ilan University, Ramat-Gan 52900,Israel
Tel: 972-3-531 8388; Fax: 972-3-5351824
E-mail: avy@mail.biu.ac.il
Some of Our Favorite Things:
1. The buccal ganglion
of Aplysia
2. Species-specific behavior
of Aplysia
3. Some recent (and not
so recent) papers (1991-present):
Ziv, I., Markovich, S., Lustig C., and Susswein,
A.J. (1991) Effects of food and mates on time budget in Aplysiafasciata:
Integration of feeding, reproduction and locomotion. Behavioral and
Neural Biology 55: 68-85.
Abstract: This study
examines the time budgeted to different behaviors in Aplysia fasciata
under three conditions: (1) animals have constant access to food and mates:
(2) there is access to food, but not to mates; (3) neither food nor mates
are present. The data suggest a number of rules underlying behavioral integration:
(1) Feeding, reproductive behaviors, and activity seem to be natural categories
for behavioral choice. Feeding and reproductive behaviors are controlled
in tandem by a common arousal mechanism, while time left over after animals
feed and reproduce is distributed in a fixed ratio between locomotion (crawling
and swimming) and inactivity (immobility and movement in place). (2) Relative
distribution between different forms of locomotion and inactivity is modified
by changes in motivational state. More time is spent swimming than crawling
when feeding and/or mating is prevented, while more time is spent moving
in place than immobile when the arousal level is increased. (3) Feedback
control of feeding and reproduction is asymmetric. Satiation of feeding
inhibits the common arousal. In the absence of food, time spent on reproductive
behaviors increases due to disinhibition of the common arousal. By contrast,
positive feedback arising from sexual behavior excites the common arousal.
When mating is prevented by removing potential mates, time spent feeding
decreases. (4) Generally, animals choose between performing the three main
categories of behavior. Although Aplysia simultaneously can feed
and mate, or locomote and mate, they do so infrequently. By contrast, different
types of reproductive behaviors (male mating, female mating, egg-laying)
are commonly performed simultaneously.
Ziv, I., Lustig C., Ben-Zion, M., and Susswein, A.J.
(1991) Daily variation of multiple behaviors in Aplysia fasciata:
Integration of feeding, reproduction and locomotion. Behavioral and
Neural Biology 55: 86-107.
Abstract: Daily variations
in feeding, reproductive behaviors, and activity level were examined under
three conditions: (1) animals had access to food and mates; (2) there was
access only to food; (3) neither food nor mates were present. Behaviors
differed in amplitude of variations from their daily mean value. Egg-laying
had the strongest tendency to be clustered. Amplitude of variations in
courtship and swimming was larger than those of immobility, crawling, and
feeding, while moving in place was the least clustered behavior. Changes
in state affected the tendency to be clustered. When food and mates were
present, amplitude of variations became progressively larger for immobility,
moving in place, crawling, and swimming. Behaviors differed in the degree
to which variations were patterned as a 1/day oscillation. Relatively little
of the variability in crawling, moving in place, courtship, and egg-laying
was due to a 1/day oscillation under any condition. By contrast, a large
proportion of the variability of immobility, swimming, mating, and eating
was modulated by a 1/day oscillation in at least one condition. The contribution
of a 1/day oscillation to variability differed in the conditions examined.
For immobility and swimming, when food and mates were present, the 1/day
component of variability became smaller. By contrast, presence of mates
led to an increase in the 1/day component of variability modulating feeding.
Daily peaks of swimming and feeding were in phase with one another, and
out of phase with mating and feeding. The ratio of locomotion to inactivity
is constant, independent of change in external conditions. However, this
ratio varied throughout the day. When food and mates were absent, variations
of immobility and swimming were strongly related to variations in the inactivity
ratio. When food and mates were added, this tendency decreased. The data
suggest that daily variations in occurrence of behaviors can be accounted
for by interactions between oscillators affecting Aplysia behavior
and motivational variables. A 1/day oscillator has strong effects on mating,
swimming, and immobility. The effect of the oscillator is modified by changes
in motivational state.
Ziv, I., Botzer, D., Markovich, S., and Susswein,
A.J. (1991) Effects of conspecifics on feeding in Aplysia fasciata.
Behavioral and Neural Biology 55: 108-113.
Abstract: The presence
of other Aplysia in the environment increases the time spent feeding.
This finding is consistent with the hypothesis that a common arousal mechanism
modulates feeding and reproductive behaviors. The arousal level is presumably
increased by pheromones released by additional animals.
Schwarz, M., Feldman, E., and Susswein, A.J. (1991)
Variables affecting long-term memory of learning that a food is inedible
in Aplysia. Behavioral Neuroscience 105:193-201.
Abstract: Long-term
memory of learning that a food is inedible was studied in Aplysia.
Seven days after a single training session, animals retained significant
memory, as measured by a number of parameters. A 2nd experiment demonstrated
savings 3 weeks after 2 training sessions. Long-term memory was also found
after training procedures were altered to resemble those more likely to
occur in nature, such as training for only 10 min or training with ad-lib
access to inedible food, with no experimenter intervention. The effects
were determined of bilaterally sectioning the esophageal nerves that innervate
the gut. Denervation of the gut blocked the ability to learn that food
is inedible but did not affect memory after the task had already been learned.
Ziv, I. Lustig, C., Markovich, S., and Susswein,
A.J. (1991) Sequencing of behaviors in Aplysia fasciata:
Integration of feeding, reproduction and locomotion. Behavioral and
Neural Biology 56: 148-169.
Abstract: To begin studying
the neural basis of higher-order decision-making in Aplysia fasciata,
we examined rules governing transitions between individual bouts of behaviors.
Sequencing between bouts was observed in a number of different conditions,
which varied with respect to access to food and/or mates. The data suggest
that a single intermediate condition, moving in place, may be centrally
related to transitions between behaviors. In all conditions, over 85% of
all transitions between behaviors were via moving in place. Moving in place
tended to precede and follow other categories of activity (crawling, swimming,
immobile), and feeding. Also, moving in place apparently represents a fixed
proportion of all bouts of behavior. In each condition, moving in place
represented ~40% of all bouts, while the number of bouts of other behaviors
varied markedly. After a bout of moving in place there was a strong tendency
for the animal to return to the behavior performed before moving in place.
Additional preferred sequences of behavior were also seen. Courtship tended
to precede mating, and crawling preceded swimming.
Botzer, D., Blumberg, S., Ziv, I., and Susswein, A.J.
(1991) Common regulation of feeding and mating in Aplysia fasciata:
Pheromones released by mating and by egg cordons increase feeding behavior.
Behavioral
and Neural Biology 56: 251-261.
Abstract: We examined
whether pheromones released by reproductive behaviors (mating and egg-laying)
affect feeding behavior. A preliminary experiment demonstrated that quantity
of food eaten can be used to measure effects of pheromones on feeding.
Using this measure, we then showed that Aplysia which were prevented
from mating, but that were in the same aquarium as mating conspecific,
eat more food than do Aplysia in a medium lacking mating animals.
Mating and feeding were not temporally correlated, indicating that pheromones
released by mating probably do not initiate feeding, but rather modulate
feeding after it has begun. Aplysia that were in the same aquarium
as freshly-deposited egg-cordons also ate more than did animals in a medium
lacking eggs.
Schwarz, M., and Susswein, A.J. (1992) Presence
of conspecifics facilitates learning that food is inedible in Aplysia
fasciata.Behavioral Neuroscience 106: 250-261.
Abstract: Feeding behavior
in Aplysia fasciata is strongly modulated by chemical stimuli signaling
the presence of a conspecific or of food in the surrounding environment.
We examined whether these stimuli also affect the ability to learn a feeding-related
task. Presence of a conspecific, but not of food, profoundly modulated
the ability to learn that food is inedible. In the absence of a conspecific,
training sessions were shorter, and no memory was exhibited upon retraining.
To distinguish whether lack of a conspecific interferes with the ability
to learn, or with the expression of memory, animals were trained in the
absence of a conspecific, and then tested in its presence. Training in
the absence of a conspecific interfered with the ability to learn. Interference
with learning was not exclusively caused by the shortened training session,
since brief training in the presence of a conspecific did lead to effective
learning. Interference with learning a food-related task could be caused
by interference with neural mechanisms for learning, or by interference
with feeding behavior. As a preliminary step in differentiating between
these 2 possibilities, we examined whether other aspects of feeding behavior
are affected by the absence of a conspecific. When a conspecific was absent,
the time needed to arouse animals with food was increased, and the number
of responses elicited by food, and the time that animals maintained responsiveness
to food, were decreased. These findings indicate that interference with
learning is likely to be caused by a decrement in the responsiveness to
food.
Hurwitz, I., and Susswein, A.J. (1992) Adaptation
of feeding sequences in Aplysia oculifera to changes in the load
and width of food. Journal of Experimental Biology 166: 215-235.
Abstract: Feeding sequences
in Aplysia are composed of a series of distinct motor acts. Foods
of differing physical or chemical characteristics produce feeding sequences
that are appropriate to the eliciting food. Rules were examined in Aplysia
oculifera for controlling how the physical characteristics of the food
modify feeding sequences. Animals were fed uniform strips of the preferred
natural food Ulva, and sequences of feeding acts in response to
this stimulus were quantified. The food was then modified, either by attaching
various weights to the end of the strip, so that animals must exert greater
force to consume the food, or by changing the width of the strip. Motor
strategy was changed in similar ways in response to both types of alteration
in the food. Inter-swallow intervals became longer and more variable, and
less food entered the mouth per swallow. In addition, some swallows partially
or completely cut the food. In some cases, the cut led to loss of contact
and release of the food. When cutting releases food, its function is apparently
to prevent food that has already been swallowed from being lost, because
it is pulled out of the interior of the animal. Cutting food may also serve
additional functions. When a cutting movement only partially cuts the food,
it is likely that the food is more easily swallowed or digested.
Chiel, H.J., and Susswein, A.J. (1993) Learning that
food is inedible in freely-behaving Aplysia californica. Behavioral
Neuroscience 107: 327-338.
Abstract: The marine
mollusc Aplysia californica can train itself that food is
inedible. Animals were given access to seaweed tied into canvas and attached
to a force transducer. Animals repeatedly found the stimulus, attempted
to ingest it, and failed. The force transducer provided an objective record
of the number of attempts made by the animal to ingest the stimulus, the
duration of each attempt, and its intensity (i.e., the peak force exerted).
Within 2.5 hours, animals showed significant declines in these three measures
of response to the stimulus. When exposed to the same stimulus the next
day, animals showed more rapid declines in responsiveness, indicating retention
of learning. Training appeared to be specific: responses of animals trained
on the seaweed Ulva to the seaweed Laurencia do not differ
from the responses of naive animals to Laurencia. Training leads
to a reduced rate of responding, which can be used as a criterion to identify
trained animals.
Levy, M., Susswein, M.O., and Susswein, A.J. (1993)
Respiratory pumping in Aplysia fasciata as part of an integrated
defensive response to increase and decrease in seawater concentration.
Journal
of Comparative Physiology A 172: 749-758.
Abstract: Much of the
neural circuitry controlling respiratory pumping in Aplysia has
been well characterized, but the function of this movement is incompletely
understood. To gain insight into possible functions of respiratory pumping,
responses were examined for a 40 min exposure to two stimuli that modulate
the movement: 1) increase and 2) decrease in seawater concentration. Thresholds
were present for both stimuli to affect respiratory pumping. Above threshold,
there were graded increases in the number of pumps elicited. There were
decrements in respiratory pump frequency as function of time exposed to
the stimulus. Increased respiratory pumping did not contribute to volume
regulation in response to exposure to altered seawaters, but was associated
with increased defensive responses, such as escape locomotion (swimming)
and inking. In addition, head shock, a well-established noxious stimulus,
elicited temporal patterns of respiratory pumping similar to those elicited
by altered seawaters. The data indicate that in our experimental condition,
respiratory pumping is elicited as part of an integrated defensive response
to noxious seawaters.
Levy, M., and Susswein, A.J. (1993) Separate neural
pathways respond to different noxious stimuli affecting respiratory pump
frequency in Aplysia fasciata. Brain Research 616: 218-229.
Abstract: Neural circuits
responsible for both conditioned and unconditioned respiratory pumping
to three stimuli modulating respiratory pumping were examined. The stimuli
used were: (i) reduction of pH; (ii) increase and (iii) decrease in seawater
concentration. Ablation of the osphradium, but not of the rhinophores,
abolished responses to all 3 stimuli. Cutting the pleural-abdominal connectives
led to a decrease in responses to lowered pH, but did not affect responses
to changes in seawater concentration. Further lesions showed that integrity
of the cerebral-pleural ganglion is needed for animals to respond to a
decrease in pH. Thus, neural circuitry entirely within the abdominal ganglion
and the periphery innervated by the ganglion is sufficient for mediating
responses to changes in seawater concentration, while the cerebral ganglion
is needed to respond to lowered pH. Different transmitter mechanisms are
also used by pathways responding to changes in seawater concentration and
to decreased pH: 5,7-dihydroxytryptamine in concentrations which cause
depletion of serotonin blocked the response to lowered pH, but not to altered
seawater concentrations.
Susswein, A.J., Markovich, S., and Achituv, Y.
(1993) Asymmetry of male and female mating in mixed-species groups of Aplysia
fasciata Poiret and Aplysia brasiliana Rang (Mollusca: Gastropoda).
Israel
Journal of Zoology 39: 213-229.
Abstract: Aplysia
fasciata and A. brasiliana are found on opposite sides of the
Atlantic Ocean, but are morphologically and behaviorally very similar.
To determine the relationship between these two species, mating patterns
were examined in same species and mixed-species groups of 2 and 4 individuals.
In single-species groups, A. brasiliana spent less time matingthan
did A. fasciata. However, the relative distribution of time spent
mating as a male, as a female, or in both sexual roles simultaneously was
virtually identical in both species. The overall time spent mating in mixed-species
groups was similar to that seen in single-species groups of A. brasiliana,
and was significantly less than in same-species groups of A. fasciata.
In mixed-species groups there were relative increases in the likelihood
for A. fasciata to mate as males, and for A. brasiliana to
mate as females. Our data indicate that when animals with differing sexual
drives are in contact, the animal with the stronger sexual drive generally
mates as a male. This suggests that the level of mating is set by a drive
to mate as a male, while female mating is largely non-selective and passive.
The data also indicate that A. fasciata and A. brasiliana are
either somewhat different populations of the same species, or are very
closely related species.
Levy, M., Markovich, S., and Susswein, A.J. (1994)
Modulation of respiratory pump rate in freely behaving pairs of Aplysia
fasciata. Behavioral and Neural Biology 61: 93-98.
Abstract: Respiratory
pumping in Aplysia is a spontaneously occurring behavior whose neural
circuitry has been explored, but whose natural functions are incompletely
understood. Respiratory pump rate was examined in freely behaving pairs
of Aplysia fasciata, to determine whether it is modified by the
occurrence mating and of other behaviors. The background rate of respiratory
pumping was ~2/hour. This rate was maintained while animals were immobile,
moving in place, crawling or feeding. The rate was increased to over 8/hour
during courtship, and to ~4/hour during female mating, and was reduced
to ~1/hour during male mating. These data suggest that respiratory pumping
has a reproductive function, perhaps in dispersal of pheromones that are
released during female mating and courtship. Respiratory pumping never
occurred while animals were swimming, suggesting that respiratory pumping
and swimming may be mutually incompatible behaviors. Respiratory pumping
was less common by night than by day.
Levy, M., Weller, A., and Susswein, A.J. (1994)
Learned changes in the rate of respiratory pumping in Aplysia fasciata
in response to increases and decreases in seawater concentration. Behavioral
Neuroscience 108: 161-170.
Abstract: In Aplysia
fasciata, shock paired with moderate increases or decreases in the
seawater concentration leads to pairing-specific increases in the respiratory
pump rate in response to the same solution an hour later. A common neural
circuit underlies learned changes to increased and decreased seawater concentration,
as shown by complete generalization of learning between these stimuli.
Different neural circuitry controls learning after pairing a shock with
pH 7.0 seawater, as shown by a lack of generalization of learning to this
stimulus. Pre-exposure to strong changes in the seawater leads to sensitization
of respiratory pumping. The hypothesis was tested that associative learning
and sensitiztion arise from activation of common pathways. However, patterns
of generalization of sensitization elicited by pre-exposure to altered
seawaters differ from those produced by associative learning.
Ziv, I., Lustig, C. Markovich, S., and Susswein
A.J. (1994) Control of individual bouts of behavior in Aplysia fasciata:
Integration of feeding, reproduction and locomotion. Israel Journal
of Zoology 40: 25-36.
Abstract: Control of
individual bouts of different behaviors was examined in Aplysia fasciata,
as part of a long-term project examining the principles underlying higher-order
decision-making. Previous studies have shown that access to food and to
mates affects the total time devoted to various behaviors. We examined
whether these factors also affect either bout lengths or bout frequencies.
Access to food inhibited mating, by decreasing both bout lengths and bout
frequencies, while access to mates increased feeding by increasing bout
length. Bouts of mobility were affected in complex ways by access to food
and mates: food had opposite effects on bout lengths and bout frequencies,
while mates decreased bout lengths.
Hurwitz, I., Goldstein, R.S., and Susswein, A.J.
(1994) Compartmentalization of pattern-initiation and motor functions in
the B31 and B32 neurons of the buccal ganglia of Aplysia californica.Journal
of Neurophysiology 71: 1514-1527.
Abstract: 1. The B31
and B32 cells in the buccal ganglia of Aplysia californica have
unusual electrophysiological features. The somata of these strongly coupled
cells do not sustain conventional action potentials. Brief depolarization
of the soma produces a complex, sustained regenerative slow depolarization
that is followed by a hyperpolarization. This activity in B31/B32 is correlated
with a patterned burst of activity expressed in many of the neurons of
the buccal ganglia. 2. Intracellular fills of B31/B32 showed that
they have many neurites adjacent to the soma, as well as peripheral axons
leaving the buccal ganglia via the radular nerve and innervating the Intrinsic-2
(I2) muscle of the buccal mass. Varicosities of B31/B32 axons are seen
within the muscle. Backfills from I2 filled two adjacent B31/B32 cells
as well as two newly identified neurons: B61 and B62. 3. Intracellular
recording from the B31/B32 axons shows that they sustain conventional action
potentials. These are recorded in the soma as approximately 10-mV fast
depolarizations. Failed spikes in B31/B32, and conventional spikes in B61/B62,
are correlated one for one with end-junction potentials (EJPs) in the I2
muscle. The EJPs are present even when the ganglia and muscles are bathed
in high-divalent cations seawater. Thus B31/B32 and B61/B62 are motor neurons
to the I2 muscle. 4. To determine whether the ability of B31/B32
to initiate patterned bursts is mediated by spikes in the axon or by slow
potentials in the soma, the B31/B32 axon was stimulated directly while
recording from the B31/B32 soma. Patterned bursts were never seen in the
absence of slow potentials in the soma. Thus the ability of B31/B32 to
initiate patterned bursts is localized to the soma and adjacent neurites.
Slow potentials influence and cause spiking in adjacent neurons even in
the absence of axon spikes. 5. These data show that the B31/B32
cells serve two functions that are compartmentalized in different regions
of the cell and are mediated via different electrical signaling mechanisms.
The B31/B32 somata utilize slow, sustained potentials as part of a network
initiating patterned activity in the buccal ganglia. The B31/B32 axons
utilize conventional action potentials, and act as motor neurons to the
I2 muscle.
Hurwitz, I., Neustadter, D., Morton, D., Chiel
, H.J., and Susswein, A.J. (1996) Activity patterns of the B31/B32 pattern
initiators innervating the I2 muscle of the buccal mass during normal feeding
movements in Aplysia californica. Journal of Neurophysiology75:
1309-1326.
Abstract: 1. B31 and
B32 are pattern-initiator neurons in the buccal ganglia of Aplysia.
Along with the B61/B62 neurons, B31/B32 are also motor neurons which innervate
the I2 buccal muscle via the I2 nerve. This research was aimed at determining
the physiological functions of the B31/B32 and B61/B62 neurons, and of
the I2 muscle. 2. Stimulating the I2 muscle in the radula rest position
produces radula protraction. In addition, in behaving animals lesioning
either the muscle or the I2 nerve greatly reduces radula protraction.
3. During buccal motor programs in reduced preparations, B31/B32 and
B61/B62 fire preceding activity in neuron B4, whose firing indicates the
onset of radula retraction. In addition, during both ingestion-like and
rejection-like patterns the activity in the I2 nerve is correlated with
protraction. 4. B31/B32 fire at frequencies of 15-25 Hz. Neither
B31/B32 nor B61/B62 elicit facilitating EJPs and EMGs in the I2 muscle.
EMGs from B31/B32 are smaller than those from B61/B62. B31/B32 and B61/B62
innervate all areas of the muscle approximately uniformly. 5. In
behaving animals, EMGs consistent with B31/B32 activity are sein the I2
muscle during the protraction phase of biting, swallowing and rejection
movements. In addition, the I2 muscle receives inputs that cannot be attributed
to either the B31/B32 or B61/B62 neurons, either because the potentials
are too large, firing frequencies are too low, or a prominent facilitation
is seen. Such potentials are associated with lip movements, and also with
radula retraction. 6. EMGs were recorded from the I2 muscle during
feeding behavior after a lesion of the I2 nerve. Animals that had severe
deficits in protraction showed no activity consistent with B31/B32 or B61/B62,
but did show activity during retraction. 7. Our data indicate that
the I2 muscle and the B31/B32 motor neurons are essential constituents
contributing to protraction movements. Activity in these neurons is associated
with radula protraction, which occurs as a component of a number of different
feeding movements. The I2 muscle may also contribute to retraction, via
activation by other motor neurons.
Hurwitz, I., and Susswein, A.J. (1996) B64, a
newly-identified central pattern generator element producing a phase switch
from protraction to retraction in buccal motor programs of Aplysia californica.
Journal
of Neurophysiology 75: 1327-1344.
Abstract: 1. Buccal
motor programs in Aplysia are characterized by two phases of activity,
which represent protraction and retraction of the radula in intact animals.
The shift from protraction to retraction is caused by synaptic activity
inhibiting neurons that are active during protraction and exciting neurons
that are active during retraction. 2. B64, a newly identified neuron
present bilaterally in the buccal ganglia, is partially responsible for
the phase shift. Stimulating a single B64 causes bilateral inhibition of
neurons B31/B32 and other neurons active during protraction, and causes
bilateral excitation of neurons B4/B5 and other neurons active during retraction.
B64 is active throughout retraction. The amplitude and waveforms of the
synaptic potentials caused by firing B64 are similar, but not identical,
to those seen during retraction. 3. Some of the effects of B64 on
B31/B32 and on B4/B5 are monosynaptic, as shown by their maintained presence
in high divalent cation seawater which blocks polysynaptic activity.
4. A brief depolarization of B64 leads to a long-lasting depolarization
and firing. The ability of B64 to respond in this way is at least partially
caused by an endogenous plateau potential, as this property is still seen
after synaptic transmission is blocked. 5. Hyperpolarization of
B64 bilaterally and preventing the somata from firing unmasks a large EPSP
in B64. This procedure does not block the shift from protraction to retraction,
indicating that spiking in the B64 somata is not necessary for the phase
shift. 6. The firing pattern and synaptic connections of B64 are
consistent with the hypothesis that the neuron is part of a central pattern
generator (CPG) underlying buccal motor programs. B64 is monosynaptically
inhibited by neurons that are active along with B31/B32, which are responsible
for producing the protraction phase of a buccal motor program. During the
later portion of the protraction phase B64 is excited. In addition, firing
B64 can phase advance and phase delay buccal motor programs. 7. Regulating
the firing of B64 can regulate the expression of buccal motor programs.
Stimulation of B64 at frequencies of 0.5 - 1.0 hz leads to complete inhibition
of buccal motor programs, while steady-state depolarization of B64 can
lead to repetitive bursts of activity.
Susswein, A.J., Rosen, S.C., Gapon, S., and Kupfermann,
I. (1996) Characterization of buccal motor programs elicited by a cholinergic
agonist applied to the cerebral ganglion of Aplysia californica.
Journal
of Comparative Physiology A 179: 509-524.
Abstract: Applying the
non-hydrolyzable cholinergic agonist carbachol (CCh) to the cerebral ganglion
of Aplysia elicits sustained, regular bursts of activity in the
buccal ganglia resembling those seen during biting. The threshold for bursting
is approximately 10-4 M. Bursting begins after a 2 to 5 min
delay. The burst frequency increases over the first 5 bursts, reaching
a plateau value of approximately 3 per minute. Bursting is maintained for
over 10 min. Some of the effects of CCh may be attributed to its ability
to depolarize and fire CBI-2, a command-like neuron in the cerebral ganglion
that initiates biting. CBI-2 is also depolarized by ACh, and by stimulating
peripheral sensory nerves. Excitation of CBI-2 caused by carbachol is partially
blocked by the muscarinic antagonist atropine. We examined whether CCh-induced
bursting is modified in ganglia taken from Aplysia that previously
experienced treatments inhibiting feeding, such as satiation, head shock
contingent or non-contingent with food, and training animals with an inedible
food. No treatment consistently and repeatedly affected the latency, the
peak burst period, the length of time that bursting was maintained, or
the threshold CCh concentration for eliciting bursting. However, there
was a decrease in the rate of the build-up of the buccal ganglion program
in previously satiated animals.
Levy, M., Levy, I., and Susswein, A.J. (1997) Respiratory
pumping in Aplysia fasciata in natural and artificial tide pools.
Journal
of Comparative Physiology A 180: 81-90.
Abstract: The rate of
respiratory pumping is gradually increased when Aplysia fasciata
are trapped in either natural or artificial tide pools, in which the oxygen
concentration, temperature, salinity and CO2
concentration are gradually changed. There are also gradual changes in
the time spent on additional behaviors. Immobility increases, while feeding
and mating decrease. Respiratory pumping is likely to contribute to the
ability of Aplysia to survive in a tide pool, since procedures causing
a decrease in the respiratory pump rate (ablation of the osphradium or
cutting the pleural-abdominal connectives) also cause an increase in the
number of animal that become moribund in the tide pool. Respiratory pumping
in artificial tide pools is triggered by a combination of all four stimuli
that are changed, but the effects caused by changes in the oxygen concentration
and temperature are the largest. Changes in other behaviors were also caused
by all of the stimuli that are altered in artificial tide pools.
Levy, M., Blumberg, S., and Susswein, A.J. (1997)
The rhinophores sense pheromones regulating multiple behaviors in Aplysia
fasciata. Neuroscience Letters 225: 113-116.
Abstract: Pheromones
released during mating and egg laying in Aplysia facilitate various
aspects of behavior. We now show that the chemosensory rhinophores sense
these pheromones. Ablating the rhinophores causes a significant decrease
in the time spent mating. In addition, the lesion blocks the increases
of feeding in response to pheromones released by egg cordons and by mating
conspecifics. Respiratory pumping is significantly increased in response
to egg cordons, mating conspecifics and egg laying hormone (ELH). The increase
in response to egg cordons is blocked by ablating the rhinophores, but
not by lesioning the osphradium, a second chemosensory organ.
Hurwitz, I., Kupfermann, I., and Susswein, A.J.
(1997) Different roles of neurons B63 and B34 that are active during the
protraction phase of buccal motor programs in Aplysia californica.
Journal
of Neurophysiology.78: 1305-1319. Download
a reprint of this paper (pdf file)
Abstract: The buccal
ganglion of Aplysia contains a central pattern generator (CPG) that
organizes sequences of radula protraction and retraction during food ingestion
and egestion. Neurons B63 and B34 have access to, or are elements of, the
CPG. Both neurons are depolarized along with B31/B32 during the protraction
phase of buccal motor programs. Both cells excite the contralateral B31/B32
neurons, and inhibit B64 and other neurons active during the retraction
phase. B63 and B34 also both have an axon exiting the buccal ganglia via
the contralateral cerebro-buccal connective. Despite their similarities,
B63 and B34 differ in a number of properties, which reflect their different
functions. B63 fires durinboth ingestion and egestion-like buccal motor
programs, while B34 fires only during egestion-like programs.
The bilateral B63 neurons, along with the bilateral B31
and B32 neurons, act as a single functional unit. Sufficient depolarization
of any of these neurons activates them all, and initiates a buccal motor
program. B63 is electrically coupled to both the ipsilateral and the contralateral
B31/B32 neurons, but monosynaptically excites the contralateral neurons
with a mixed electrical and chemical EPSP. Positive feedback caused by
electrical and chemical EPSPs between B63 and B31/B32 contributes to the
sustained depolarization in B31/B32 and firing of B63 during the protraction
phase of a buccal motor program.
B34 is excited during the protraction phase of all buccal
motor programs, but unlike B63, it does not always reach firing threshold.
The neuron fires in response to current injection only after it is depolarized
for 1 - 2 sec, or following preceding buccal motor programs in which it
is depolarized. Firing of B34 produces facilitating EPSPs in the contralateral
B31/B32 and B63 neurons, and can initiate a buccal motor program. Firing
in B34 is strongly correlated with firing in the B61/B62 motor neurons,
which innervate the muscle (I2) responsible for much of protraction. B34
monosynaptically excites these motor neurons. B34 firing is also correlated
with firing in motor neuron B8 during the protraction phase of a buccal
motor program. B8 innervates the I4 radula closer muscle, which in egestion
movements is active during protraction, and in ingestion movements is active
during retraction. B34 has a mixed, but predominantly excitatory effect
on B8, via a slow conductance-decrease EPSP. Thus, firing in B34 leads
to amplification of radula protraction that is coupled with radula closing,
a pattern characteristic of egestion.
>Blumberg, S., and Susswein, A.J. (1998)
Consummatory feeding movements in Aplysia fasciata are facilitated
by conspecifics with access to mates, by reproductive tract homogenates
and by bag cell peptides. Journal of Comparative Physiology A. 182:
175-182.
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file)
Abstract: In Aplysia
fasciata, pheromones released by conspecifics with access to mates
increase the quantity of food eaten. This effect is blocked when the chemosensory
rhinophores are ablated, indicating that the rhinophores sense pheromones.
The modulation of feeding by pheromones can be monitored by an increased
in the amplitude of swallowing movements in presence of conspecifics with
access to mates. Atrial gland homogenates and four bag cell peptides (ELH
- egg laying hormone, and a, b, and g bag cell peptides) amplify the swallow
amplitude in a manner similar to that caused by conspecifics with access
to mates, suggesting that peptides from the bag cell/atrial gland family
that are released from the atrial gland into the surrounding water may
be pheromones regulating feeding and reproductive behaviors.
Nedvetzki, Y., Markovich, S., and Susswein,
A.J. (1998) Inhibition of mating in Aplysia fasciata by food stimuli
in the environment, but not by post-ingestion stimuli causing satiation.
Journal
of Comparative Physiology A. 182: 183-190.
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(pdf file)
Abstract: Aplysia
mating is inhibited when animals have steady-state access to food. We examined
which stimuli provided by food inhibit mating. Pre-feeding animals to satiation
caused a decrease in mating immediately after the meal. This effect could
be mimicked by placing food into the water for the length of time of a
meal just before the animals were allowing to mate, but not by filling
the gut with non-nutritive bulk, which inhibits feeding. The presence of
food in the water while animals were allowed to mate caused a stronger
inhibition of mating. When food was maintained in the water for 24 hours,
animals adapted to this stimulus, indicating that the maintained presence
of food could not alone account for the inhibition of mating in steady-state
conditions of access to food. However, food in the water for 24 hours,
coupled with an occasional touch of food to the lips while animals had
access to mates, caused strong inhibition of mating. We tested the hypothesis
that food initiates a state of food arousal, which competes with sexual
arousal, and thereby inhibits mating. If this hypothesis is correct, gut
fill should facilitate mating, by inhibiting food arousal. However, this
effect was not observed. The data support the hypothesis that food stimuli
directly inhibit sexual arousal, rather than acting via an excitation of
food arousal.
Blumberg, S., Haran, T., Botzer, D., Susswein,
A.J., and Teyke, T. (1998) Pheromones linked to sexual behaviors excite
the appetitive phase of feeding behavior in Aplysia fasciata. I.
Modulation and excitation of appetitive behaviors. Journal of Comparative
Physiology A 182: 777-783.
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(pdf file)
Abstract: Pheromones
secreted by mating conspecifics - as well as homogenates containing tissue
that is homologous with the atrial gland - increase the time that Aplysia
fasciata spent feeding. This effect is caused by increasing the number
of feeding episodes initiated in response to food, whereas the length of
a feeding bout remains unchanged. The increase in the number of feeding
episodes is related to increases in head waving and crawling, i.e., appetitive
movements that bring the animal into contact with food, as well as an increase
in the responsiveness to food after it is contacted. Releasing a homogenate
containing atrial gland tissue, or egg laying hormone (ELH), in the water
near the animal, elicited head lifting similar to that seen when animals
are food aroused. The data indicate that the facilitation of Aplysia
feeding caused by pheromones arises in part by an excitation of appetitive
behaviors. These findings suggest that neurons generating appetitive behaviors
will be affected by pheromones.
Teyke, T., and Susswein, A.J. (1998) Pheromones
linked to sexual behaviors excite the appetitive phase of feeding behavior
in Aplysia fasciata. II. Excitation of C-PR, a neuron involved in
the generation of appetitive behaviors. Journal of Comparative Physiology
A. 182: 785-791.
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Abstract: Pheromones
released by conspecifics amplify both the appetitive and the consummatory
components of feeding in Aplysia. These effects can be mimicked
by applying homogenate of the large hermaphroditic duct (LHD) containing
atrial gland tissue, as well as peptides from the bag cells. Identified
cerebral neuron C-PR of Aplysia is thought to command various behaviors
that comprise the appetitive phase of feeding. In a reduced preparation,
we investigated the effects on neuron C-PR of applying these substances
to the rhinophores, which sense pheromones. Stimuli that excite feeding
in the animal were also found to affect C-PR. LHD homogenate caused a doubling
in the firing rate of the C-PR. LHD homogenate also amplified the response
of the C-PR to other excitatory stimuli, such as touch of food to the rhinophores.
Bag cell peptides (ELH and a, b
and g bag cell peptide) caused smaller increases
in the firing rate of the C-PR. These data are consistent with the hypothesis
that pheromones initiate appetitive feeding behavior in part via their
excitation of C-PR.
Schwarz, M., Blumberg, S., and Susswein, A.J
(1998) Social isolation blocks the expression of memory
following training that a food is inedible in Aplysia fasciata. Behavioral
Neuroscience. 112: 942-951.
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file)
Abstract: Isolating
a sexually mature Aplysia fasciata for either one or twenty-four
hours immediately after training that a food is inedible blocks the subsequent
expression of memory measured 24 hours later. Isolation that is delayed
for an hour following training, but not for 12 hours after training, is
also effective in blocking memory. Isolation affects memory because of
a specific effect caused by the absence of pheromones secreted by conspecifics,
rather than by a non-specific change in the chemical environment, since
transferring animals to a novel environment (120% seawater) that contains
a conspecific does not affect memory. Isolation also does not affect memory
in sexually immature Aplysia, even though immature animals are able
tosense one another’s presence. Isolation may affect memory because social
(and sexual) isolation is a form of stress in mature A. fasciata,
and stress after training affects retention in many animals.
Botzer, D., Markovich, S., and Susswein, A.J.
(1998) Multiple memory processes following training that a food is inedible
in Aplysia. Learning & Memory. 5: 204-219.
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Abstract: In many organisms,
memory after training can be separated into a number of processes. We now
report that separable memory processes are also initiated by a training
procedure affecting Aplysia feeding behavior, a model system for
examining the neural mechanisms underlying the regulation of a complex
behavior. Four distinct memory processes were identified: 1) A very short
term memory that declines within 15 min. 2) A short-term memory that persists
for 0.5 – 1.0 hours. 3) An intermediate-term memory, observed 4 hrs after
training. 4) A long-term memory that is seen only after a 12 – 24 hour
delay. The 4 memory processes can be distinguished by the different training
procedures that are required to elicit them. A single 5 minute training
session is sufficient to elicit the very short-term memory. However, a
longer training session that continues until the animal stops responding
to food is needed to elicit short–term memory. Intermediate term memory
is observed only after a spaced training procedure (three 5 minute training
sessions separated by 30 minute intervals). A single 5 minute training
session which does not cause either short-term or intermediate-term memory
is sufficient to induce long-term memory, indicating that short- and long-term
memory are independent, parallel processes. Short- and long-term memory
can also be separated by the effects of a post-training experience. Long-term,
but not short-term memory, can be attenuated by cooling animals immediately
after training. Cooling prior to the training does not affect either the
training or the subsequent short- or long-term memory.
Levy, M., and Susswein, A.J. (1999) Separate
effects of a classical conditioning procedure on respiratory pumping, swimming
and inking in Aplysia fasciata. Learning & Memory.
6:
21-36.
Download a reprint of this paper (pdf
file).
Abstract: We examined
whether swimming and inking, two defensive responses in Aplysia fasciata,
are facilitated by a classical conditioning procedure that has been shown
to facilitate a third defensive response, respiratory pumping. Training
consisted of pairing a head shock (UCS) with a modified seawater (85%,
120% or pH 7.0 seawater - CSs). Animals were tested by re-exposing them
to the same altered seawater one hour after the training. For all three
altered seawaters, only respiratory pumping is specifically increased by
conditioning. Swimming is sensitized by shock, and inking is unaffected
by training, indicating that the conditioning procedure is likely to affect
a neural site that differentially controls respiratory pumping. Additional
observations also indicate that the three defensive responses are differentially
regulated. First, different noxious stimuli preferentially elicit different
defensive responses. Second, the three defensive responses are differentially
affected by shock. Inking is elicited only immediately following shock,
whereas swimming and respiratory pumping are facilitated for a period of
time following the shock. Third, swimming and respiratory pumping are differentially
affected by noxious stimuli that are delivered in open versus closed environments.
These data confirm that neural pathways exist which allow Aplysia
to modulate separately each of the three defensive behaviors that were
examined.
Hurwitz I., Cropper E.C., Vilim, F.S., Alexeeva
V., Susswein A.J., Kupfermann I., and Weiss, K.R. (2000) Serotonergic and
peptidergic modulation of the buccal mass protractor muscle (I2) in Aplysia.
Journal of Neurophysiology 84: 2810-2820.
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Abstract: Plasticity
of Aplysia feeding has largely been measured by noting changes in
radula protraction. On the basis of previous work, it has been suggested
that peripheral modulation may contribute to behavioral plasticity. However,
peripheral plasticity has not been demonstrated in the neuromuscular systems
that participate in radula protraction. Therefore in this study we investigated
whether contractions of a major radula protraction muscle (I2) are subject
to modulation. We demonstrate, first, that an increase in the firing frequency
of the cholinergic I2 motoneurons will increase the amplitude of the resulting
muscle contraction but will not modulate its relaxation rate. We show,
second, that neuronal processes on the I2 muscle are immunoreactive to
myomodulin (MM), RFamide, and serotonin (5-HT), but not to small cardioactive
peptide (SCP) or buccalin. The I2 motoneurons B31, B32, B61, and B62 are
not immunoreactive to RFamide, 5-HT, SCP, or buccalin. However, all four
cells are MM immunoreactive and are capable of synthesizing MMa. Third,
we show that the bioactivity of the different modulators is somewhat different;
while the MMs (i.e., MMa and MMb) and 5-HT increase I2 muscle relaxation
rate, and potentiate muscle contraction amplitude, MMa, at high concentrations,
depresses muscle contractions. Fourth, our data suggest that cAMP at least
partially mediates effects of modulators on contraction amplitude and relaxation
rate.
Last Update: December 31, 2000