Integrative and Comparative Biology
Integrative and Comparative Biology, volume 53, number 2, pp. 183–191
doi:10.1093/icb/ict073
Society for Integrative and Comparative Biology
INVITED REVIEW
Toward an Organismal Neurobiology: Integrative Neuroethology
Richard A. Satterlie1
Department of Biology and Marine Biology and Center for Marine Science, University of North Carolina Wilmington,
5600 Marvin K. Moss Lane, Wilmington, NC 28409, USA
1
E-mail: [email protected]
Synopsis Overt behavior is generated in response to a palette of external and internal stimuli and internal drives. Rarely
are these variables introduced in isolation. This creates challenges for the organism to sort inputs that frequently favor
conflicting behaviors. Under these conditions, the nervous system relies on established and flexible hierarchies to produce
appropriate behavioral changes. The pteropod mollusc Clione limacina is used as an example to illustrate a variety of
behavioral interactions that alter a baseline behavioral activity: slow swimming. The alterations include acceleration
within the slow swimming mode, acceleration from the slow to fast swimming modes, whole body withdrawal (and
inhibition of swimming), food acquisition behavior (with a feeding motivational state), and a startle locomotory
response. These examples highlight different types of interaction between the baseline behavior and the new behaviors
that involve external stimuli and two types of internal drives: a modular arousal system and a motivational state.
The investigation of hierarchical interactions between behavioral modules is a central theme of integrative neuroethology
that focuses on an organismal level of understanding of the neural control of behavior.
A long-standing goal of neuroethology is to understand behavior in terms of neuronal interconnections, neuronal properties, modulatory influences,
and effector activities, and this has embraced
approaches from the molecular and genomic to the
biomechanical and the ecological, including mathematical modeling and engineering of biomimetic
robotics. Despite an apparent reductionist direction
of much of this research, the emphasis has remained
on behavior, and thus on the actions and reactions
of the organism within its environment.
This places neuroethology squarely within the
umbrella of the Grand Challenges in Organismal
Biology (Schwenk et al. 2009), where an emphasis
on the performance of the organism within its environment provides a substrate for natural selection.
However, selective pressures likely are not exerted
on individual behaviors in isolation. Rather, the
interplay between behavioral modules frequently determines the ‘‘fitness’’ of an individual or of a population of individuals placed in situations of
environmental change. This interplay, whether
short-term or long-term, involves a suite of internal
drives and internal and external stimuli, which must
be integrated to sort between competing behaviors,
to produce blended behaviors, or to generate unique
or innovative responses. This can involve a continuum from ‘‘hard-wired’’ hierarchies, through
conditional hierarchies, to blended or unique behaviors. Indeed, maladapted behavioral responses can
threaten a species just as effectively as maladapted
reproductive or developmental strategies, morphological features, or physiological processes.
This broader approach of neuroethology is important not only at the individual and population levels
but also at the comparative level. Everything from
the hard-wired to the most flexible of hierarchies
can be investigated from the genomic and molecular
levels to the ecosystem levels, with time-courses from
fractions of seconds to generations. How these hierarchies sort out in response to immediate and
longer-term environmental changes could determine
the ultimate fate of the organisms themselves.
Most animals must locomote (excepting sessile species), and all must obtain food, escape from danger or
defend themselves, seek mates and reproduce, successfully develop to maturity, and use past experience to
shape future behaviors. The internal and external stimuli and internal drives related to these needs do not
arrive in isolation or in a ‘‘single-file’’ presentation,
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184
like the considerate movie ninjas who pause to attack
the hero one-at-a-time. Therefore, it is critical for the
organism to make decisions based on what could be
considered conflicting stimuli that require an integrative alteration of, or change from, ongoing behavior.
The investigation of this behavioral variability does not
need an ‘‘omics’’ label since it is already fully encompassed within the field of Neuroethology. Certainly,
there is nothing magical in this suite of organismal
needs, but it takes on a sense of wonder when we
look at the tremendous diversity of biological solutions
for filling these needs.
An animal’s sensory world consists of a complex
blend of variables, but the interpretation of these
inputs is also dependent on less straightforward
internal states. Tinbergen (1951) first noted that
internal or motivational states of an animal can produce variability in overt behavioral patterns. In order
to understand how motivational states and arousal
systems modulate behavioral choice, it is necessary to
examine proximate causal mechanisms underlying
these behavioral phenomena (van Staaden and
Huber 2001). This requires a shift from an investigation of neural mechanisms that produce a particular behavior to a ‘‘higher level’’ understanding of a
neural environment that alters the probability that a
specific behavior will be expressed (Kravitz 1988). In
this context, arousal and motivation refer to reversible, short-term behavioral modulators that are not
associated with fatigue or learning. Furthermore,
arousal and motivational systems are assumed to
have an integrity honed through evolutionary selection rather than through the life experiences of an
organism (van Staaden and Huber 2001). The situation is not a simple one. At any specific time, a
variety of parallel arousal mechanisms, some competing, some complementary, can provide simultaneous
modulatory inputs that, together, produce a behavioral response appropriate for the particular sensory
(internal and external) context.
Invertebrate preparations have provided significant
contributions to our understanding of the integration of internal states and internal and external
stimuli. A few examples from this area of integrative
neuroethology include reconfiguration of neural circuits by motivational states (Jing and Weiss 2005;
Jing et al. 2007), the impact of aggressive states
and social status on behavioral hierarchies
(Edwards and Kravitz 1997; Kravitz and Huber
2003), sequential decision-making and population
codes in behavioral choice (Kristan and Shaw 1997;
Esch et al. 2002), and alternation of the value and
impact of sensory inputs by internal modulation
(Certel et al. 2007; Tsunozaki et al. 2008).
R. A. Satterlie
Fig. 1. Live specimen of Clione limacina with buccal cones (BCs)
everted and grasping a shelled pteropod (P). W, wing; T, tail.
One invertebrate species will be used here to illustrate some of the types of behavioral decisions that
must be made based on external and internal stimuli
and internal drives. This animal, the pteropod mollusc Clione limacina (Fig 1), is convenient for these
types of investigation because it displays a ‘‘baseline
behavior’’ that is nearly continuous except during
periods of downward vertical migration. That behavior is slow swimming (Arshavsky et al. 1985a;
Satterlie et al. 1985). From that baseline, we can describe several behavioral modifications that alter slow
swimming, including some that are mutually exclusive, and some that alter swimming either directly or
as a component of a separate behavioral entity. Some
of the results are obvious. Mutually exclusive behaviors should inhibit one another, but one focus of
neuroethology is on how that inhibition is structured
within the circuitry, interactions, and cellular properties of the component neurons. Through a
comparative approach to similar hierarchical decision-making, both common and unique solutions
may emerge, along with an evaluation of their relative successes in dealing with internal and environmental change.
As a backdrop to the swim-system story, Clione
are typically observed in the slow swimming mode.
This is an upward-directed locomotion, that either
maintains position in the water column or slowly
moves the animal upward or even with a loss of
vertical position (Satterlie et al. 1985). Even this
latter downward movement is considered forward
locomotion since the animal is negatively buoyant
and swimming partially overcomes the downward
gravitational force.
Integrative neuroethology
In a theoretical sense, acceleration of swimming
can occur in at least three primary ways: through
an increase in the frequency of appendages movements, through an increase in the strength of movements of appendages, and through biomechanical
changes in the movements of appendages. The
focus here will be on the first two.
Three types of acceleration during swimming have
been described for Clione: (1) acceleration within the
slow swimming mode, (2) acceleration from slow to
fast swimming, and (3) a startle-response lunge. The
first can be triggered by mild stimulation of a wing
(parapodium) or the body wall, and is seen in nature
when the animal makes contact with other animals
or small debris in the water column. The primary
characteristic of acceleration within slow swimming
is an increase in the force of wing movements without an increase in the frequency of wing-beat. The
result is a slight increase in the rate of forward
(upward) movement (Arshavsky et al. 1985a;
Satterlie and Spencer 1985).
The acceleration from slow to fast swimming is typically sudden and dramatic, and is produced by strong
(but not damaging) stimulation of the tail or body wall.
From the ‘‘treading water’’ or slight upward movement
of slow swimming, the animal moves upward at rates as
high as two or three body lengths per second. This is
accomplished by an increase in frequency of wing-beat
(from around 1 to 3–4 Hz), a dramatic increase in the
force of wing movements, and in a change of the angle
of attack of the wings. The neural substrates of these
changes are summarized below.
The startle-response is triggered by nociceptive
stimulation of the tail, and involves two or three
rapid wing-beats that propel the animal to an extrapolated speed of over 15 body lengths/s (Satterlie et al.
1997). This is extrapolated because the startle-response produces a forward lunge that lasts less
than 1 s, after which the animal continues its
escape in the fast swimming mode.
Two additional responses should be noted. With
stimulation of the head or neck, swimming is inhibited, the wings are retracted into the body, and
the body shortens in what is called a whole-body
withdrawal (Norekian and Satterlie 1996a, 1996b).
This results in passive sinking, head first, away
from the stimulus. After a few seconds, swimming
resumes and with bending of the rudder-like tail, the
animal returns to normal head-upward swimming.
Stimulation of a wing can trigger retraction of that
wing, retraction of both wings, and inhibition of
swimming (Huang and Satterlie 1990). These responses have a higher threshold than does the
185
stimulation of the wing that produces acceleration
of slow swimming.
The baseline behavior—slow swimming
The slow swimming rhythm is generated by a twophase central pattern generator (CPG) in which
groups of ‘‘upswing’’ and ‘‘downswing’’ interneurons
interact with reciprocal inhibitory connections. All
interneurons in each group are electrically coupled,
and all interneurons produce a single, broad action
potential in their appropriate half-cycle (Arshavsky
et al. 1985a, 1985b, 1985c; Satterlie and Spencer
1985). Postinhibitory rebound in the neurons adds
to the stability of the rhythm (Satterlie 1985).
CPG interneurons excite agonistic motorneurons
and inhibit antagonistic motorneurons (Arshavsky
et al. 1985a, 1985b; Satterlie and Spencer 1985;
Satterlie 1993). The motorneurons have relatively
small cell bodies (up to 30 mm) and selectively innervate slow-twitch swim muscle within restricted innervation fields of the ipsilateral wings. The small
motorneurons of each pedal ganglion (30–40 neurons) are roughly equally divided between dorsal
and ventral innervation of muscle, and each produces a burst of action potentials in its appropriate
half-cycle. Slow-twitch muscle cells receive monosynaptic input from motorneurons and produce either a
single junctional potential or spike-like response per
swim contraction (Satterlie 1991, 1993). Both types
of electrical responses are variable in amplitude,
which is directly related to the strength of
contraction.
Change #1. Reflex-type activities:
acceleration within the slow swimming
mode and wing-withdrawal
Mild tactile stimulation of a wing triggers an increase in
the force of the wing’s contractions without an associated increase in frequency of wing-beat (Satterlie, in
preparation). Wing mechanoreceptors produce bursts
of action potentials with each stimulus, and these are
capable of inducing two reflex behaviors: acceleration
of swimming and withdrawal of the wing (with inhibition of swimming). The common sensory inputs rely
on differences in threshold for these reflexes, which do
not appear to be fully mutually exclusive (swimming
with enhanced contractions can be observed with partial retractions of the wing).
Sensory cell bursts activate symmetrical clusters of
serotonergic neurons in the pedal ganglia via polysynaptic connections (Fig. 2; Satterlie, in preparation). The serotonergic clusters include neurons
that innervate the swim musculature of the ipsilateral
186
R. A. Satterlie
Fig. 2. Dual recording from a sensory neuron (S) in the wing and a pedal serotonergic neuron (5-HT). Each of the three bursts in the
sensory cell is triggered by mechanical stimulation of the ipsilateral wing, and each burst induced a similar burst of action potentials in
the serotonergic neuron, which modulates the swim musculature of the ipsilateral wing to enhance swim contractions.
wing and produce modulatory enhancement of the
wings’ contractions. The serotonergic cells do not
produce central inputs to any other components of
the swim system—their modulatory influence is
strictly peripheral, and they selectively modulate the
slow-twitch muscle. This reflex circuit increases the
wings’ contractility and is proposed as one means of
producing acceleration within the slow swimming
mode (Satterlie, in preparation).
The same sensory cells activate the wings’ withdrawal circuit by stimulating a pair of wing-withdrawal interneurons that act as gateway neurons
for subsequent activation of the wing-withdrawal
musculature of the ipsilateral wing (lateral and longitudinal retractor muscle and dorsoventral muscle—
all of the smooth type) (Huang and Satterlie 1990).
The interneurons extend processes to both pedal
ganglia and innervate populations of withdrawal
motorneurons to mediate either ipsilateral or bilateral withdrawals of the wings, depending on the
strength and the number of the stimuli. Swimming
is inhibited with full withdrawals of the ipsilateral
wing and with bilateral withdrawals. Expansion of
the wings following withdrawal is slow and presumably due to hemostatic re-inflation of the hemocoel
of the wing. Swim contractions typically resume
before the wings are fully expanded.
Change #2. Fast swimming: activation of
a modular arousal system
Firm stimulation of the tail or body wall of a slowswimming animal triggers a sudden acceleration that
is equivalent to a gait change for Clione (Arshavsky
et al. 1985a, 1985b, 1985c; Satterlie and Spencer
1985). As mentioned above, acceleration is produced
by an increase in the frequency of wing-beat, a dramatic increase in the wings’ contractility, and a
change in the angle of attack of the wings (Szymik
and Satterlie 2011). The change can also be initiated
by bath-applying serotonin to a dissected animal,
and the bout of fast swimming will continue until
the serotonin is washed out.
Direct stimulation of neurons from two symmetrical clusters of serotonergic cells of the cerebral
ganglia is capable of producing the full suite of
changes characteristic of the slow-to-fast acceleration
(Satterlie 1995; Satterlie and Norekian 1995, 2001;
Satterlie et al. 1995). These cells oversee a reconfiguration of the swim CPG through recruitment of an
additional pair of interneurons that directly shorten
the interpulse intervals of CPG activity and thus increase the frequency of wing-beats (Fig 3; Arshavsky
et al. 1985d, 1989b; Pirtle and Satterlie 2007). The
cerebral serotonergic cells also promote recruitment
of symmetrical pairs of large motorneurons (Fig. 4;
two per pedal ganglion, one each innervating the
ipsilateral dorsal and ventral swim muscles, respectively). The large motorneurons innervate fast-twitch
fatigable swim musculature, so their activity results
in recruitment of the full complement of the swim
musculature. In addition, the cerebral serotonergic
neurons enhance the ongoing activity of the small
motorneurons and thus the slow-twitch musculature.
Finally, the cerebral cells also activate the pedal clusters of serotonergic neurons that produce the peripheral modulation of the slow-twitch muscle during
acceleration in the slow swimming mode. This
three-headed excitation of the swim musculature creates the dramatic increase in wing contractility characteristic of the change from slow to fast swimming
(Satterlie and Norekian 1995, 1996, 2001; Pirtle and
Satterlie 2004).
As part of the fast-swim acceleration, the cerebral
serotonergic neurons also activate a heart excitor
neuron in the left pedal ganglion and inhibit the
whole-body-withdrawal neurons (described below).
We already know that the pedal serotonergic neurons
can act independently for acceleration in the slow
swimming mode. Similarly, the heart excitor
Integrative neuroethology
187
Fig. 3. Intracellular recording from a CPG interneuron (Int) and an extracellular recording from the ipsilateral wing nerve
(Wing Nerve). At the arrow, a bout of fast swimming is triggered. Note the increase in CPG cycle frequency. Also, the recording
from the wing nerve shows a recruitment of large units with the acceleration.
neuron is active in situations other than the acceleration to fast swimming. It thus appears that this
overall arousal system is modular in construction;
individual modules can be activated independently,
but also called into activity together during fast
swimming (Satterlie and Norekian 1996, 2001).
Change #3. Choice between mutually
exclusive behaviors: whole-body
withdrawal.
A symmetrical pair of interneurons has been identified in the pleural ganglia that produce all of the
behavioral responses characteristic of whole-body
withdrawal: contraction of the musculature of the
tail, body wall, neck, and head to ‘‘round up’’ the
animal; full withdrawal of the wings; and inhibition
of all swimming activity (Fig. 5; Norekian and
Satterlie 1996a). Forceful mechanical stimulation of
the head or neck is most effective in producing the
response, which has a high threshold for activation.
The withdrawal interneurons send processes to all
central ganglia and peripheral regions of the body.
They synaptically inhibit swim motorneurons and
receive inhibitory inputs from the cerebral serotonergic cells that induce fast swimming (Norekian and
Satterlie 1996b). Thus, these mutually exclusive behaviors have reciprocal inhibitory connections, such
that fast swimming can suppress whole-body withdrawal, but with sufficient stimulation, activation of
the whole-body-withdrawal neurons will turn off
swimming and allow passive sinking (Norekian and
Satterlie 2001a).
Additional inhibitory inputs to the withdrawal interneurons come from the food-acquisition system
(described below), so feeding takes precedence over
whole-body withdrawal (Norekian and Satterlie
1995). We can define this hierarchy as food-acquisition4whole-body withdrawal4slow swimming, in
which the switch between whole-body withdrawal
and fast swimming is a matter of the relative
strengths of stimuli.
Change #4. Activation of a motivational
state: food-acquisition behavior
Clione are feeding specialists, eating only shelled
pteropods. As active predators feeding on active
prey, they have an extremely specialized method of
capturing prey. Six tentacle-like buccal cones are
held, uninflated, inside the mouth. With proper
stimulation, the buccal cones are hydraulically inflated to a length equal to about one-half of the animal’s body length, and this is achieved in 50 ms
(Fig. 1) (Hermans and Satterlie 1992). The buccal
cones are used to grab the prey, which is then manipulated so that the opening of the shell is over the
mouth, and the prey is consumed (mechanisms of
the extraction of prey are not discussed here).
The stimuli that trigger the capture of prey are interesting. If a relatively weak mechanical stimulus is
delivered to the head, in the region of the mouth, a
local muscular withdrawal pulls the stimulated patch
of skin away from the stimulating object (Arshavsky
et al. 1989a; Norekian 1993, 1995; Norekian and
Satterlie 1993a, 1995). If the animal is first exposed to
188
R. A. Satterlie
Fig. 4. Dual recording from a large motorneuron (Lmn) and a small motorneuron (Smn). At the arrow a bout of fast swimming is
triggered. Note that the large motorneuron only received depolarizing and hyperpolarizing synaptic input prior to the acceleration, but
is recruited into firing activity at the change. Also note the increase in cycle frequency with the acceleration. The small motorneurons
receive the same type of synaptic input from the CPG, but they produce bursts of action potentials with each depolarizing input in both
slow and fast swimming modes.
Fig. 5. Wing-withdrawal neurons have large cell bodies (40 mm in
diameter) in the pleural ganglia and send axon branches to all
central ganglia and to the periphery.
a chemical extract of the prey (made by grinding up the
soft tissues of a shelled pteropod), or if a live prey is
brought near the oral region, exactly the same mechanical touch triggers the ballistic eversion of the buccal
cones for a full acquisition-reaction. Eversion of the
buccal cones is accompanied by activation of fast swimming, inhibition of statocyst control of swimming so
the animal swims in irregular loops and turns, and an
initial forward lunge that is similar to the startleresponse.
With the chemical stimulus, the value of the
mechanoreceptor input is altered so a local withdrawal response is converted to full-fledged foodacquisition behavior that includes recruitment of
several behavioral modules. This change in the qualitative value of the mechanoreceptor’s input is considered a component of a feeding motivational state
that also alters the other behavioral modules.
The neural circuitry for eversion and retraction of
the buccal cones has been described, and the mechanism for the ballistic nature of the eversion has been
determined (Arshavsky et al. 1989a; Norekian 1993,
1995; Norekian and Satterlie 1993a, 1993b, 1995).
With nonmotivated mechanical stimulation, the
buccal-cone-retraction neurons increase their activity, ensuring that a reaction by the buccal cones is
not generated (Fig. 6A). With chemical stimulation
of the motivational state, similar mechanical stimulation produces an initial co-contraction of the eversion and retractor motorneurons, which builds
pressure within the head hemocoel (Norekian and
Satterlie 1993b). A subsequent inhibition of the retractor motorneurons, together with enhanced firing of
the eversion motorneurons, produces the ballistic inflation of the buccal cones (Fig. 6B).
The mechanoreceptors and chemoreceptors that
participate in food-acquisition behavior have not
yet been identified, so the mechanism of alteration
of the value of mechanoreceptor input by the feeding
motivational state is not yet known.
Change #5. Independent activation of
common locomotory musculature: the
startle-response
As mentioned above, nociceptive mechanical stimulation delivered to the tail or body wall during slow
swimming activates extremely powerful contractions
of the swim musculature to produce a startle-lunge.
Integrative neuroethology
189
Fig. 6. Dual recordings from buccal-cone-eversion motorneurons (LA1 and RA1: L and R refer to right and left), and buccal-coneretractor motorneurons (LB1 and RB1). (A) A mechanical touch to the head in the absence of chemical activation of the feeding
motivational state only produced a local withdrawal response. The increased firing in the retractor motorneuron and weak firing in the
eversion motorneuron maintains the buccal cones in the retracted state. (B) An identical mechanical stimulus to the head following
chemical (prey extract) activation of the feeding motivational state, results in co-firing of eversion and retractor motorneurons
(and thus co-contraction of the antagonistic musculature), followed by a sudden inhibition of the retractor motorneuron. This creates a
ballistic eversion of the buccal cones.
This ballistic response is followed by an extended
period of fast swimming. Two symmetrical pairs of
large motorneurons (up to 50 mm cell body diameter)
monosynaptically activate both types of swim muscle
to produce the powerful contractions (Satterlie et al.
1997). The motorneurons are controlled by a symmetrical pair of cerebral interneurons, via both chemical
and electrical synapses (Norekian and Satterlie 1997).
The interneurons are activated by mechanoreceptors in
the tail and body wall.
Activity in the startle-neurons (interneurons and
motorneurons) is not phase-locked with CPG activity
so the startle is immediately initiated regardless of the
swimming phase. The startle system also stimulates the
swim system to produce the extended period of fast
swimming. In this case, the startle-response temporarily overrides the swim system before returning control
in the fast-swimming mode.
The startle neurons not only receive excitatory
input from the mechanoreceptors in the body but
also receive excitation from the food-acquisition
system (Norekian and Satterlie 1997). Thus, a startle-like lunge accompanies eversion of the buccal
cones to help capture prey, and adds the startle
190
behavioral module to the multi-module food-acquisition behavior.
Conclusions
This brief survey of the behavioral responses of
Clione, and their neuronal mechanisms of control,
shows how several behavioral changes involve both
external stimuli and internal drives in altering and
overriding an ongoing behavior, based on relatively
rigid and moment-to-moment hierarchies. This includes use of a modular serotonergic arousal system
that is involved, in part or in full, in several behavioral responses. As expected, mutually exclusive behaviors interact via reciprocal inhibitory connections,
but they still exhibit an hierarchical order.
One aspect of the Clione system that has not yet
been investigated is the potential for modification
of these various responses based on past experience
(¼ learning). This type of behavioral modification
elevates the time-course of behavioral modification
as much as it holds the potential to alter the existing
interactions between external and internal stimuli
and internal drives.
These larger-scale, integrative analyses of neuroethological processes fully encompass the spirit of
the Grant Challenges in Organismal Biology, and
find traction in each of the five specific challenges
collectively summarized by Schwenk et al. (2009).
Neuroethology, by its very definition, is about the
organism and its relationship with its environment.
By taking a more integrative look at behavioral control and behavioral variability, we can better understand the internal and external worlds of the
organism. This approach is not new. The summary
of Clione’s behaviors is just one example, forwarded
here to draw attention to a more integrative approach to neuroethology, and its value in better
understanding the organism.
Acknowledgments
This review is based on a presentation of the Plenary
Lecture at the January 2013 annual meeting of the
Society for Integrative and Comparative Biology (San
Francisco, CA, USA). I thank the Executive
Committee and the Society President and Secretary,
Drs Ken Sebens and Lou Burnett, for the invitation
to give the talk and to write this article. The work
was supported by grants from the National Science
Foundation and the National Institute of Health.
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