Neurobiology 303 -- Chapter 19 Outline

Mechanisms of escape behavior

behavior can be viewed as an overt expression of the integrating action of
   the nervous system
    integration in the nervous system involves:
       reception of sensory stimuli
       processing of those sensory inputs
       consideration of prevailing circumstances
       production of an appropriate motor response

escape behavior is an appropriate subject for the study of integration in the
   nervous system because:
       it's relatively simple but involves many neural decisions
       it's readily observed in the laboratory or in the field
       it's crucial for the survival of all organisms

an excellent example of a well-studied escape behavior is that of the
    avoidance of bat predators by nocturnal (noctuid) moths
    we will consider different aspects of this avoidance which include:
       how moths hear the ultrasonic cries of bats
       how they use that sensory input to make behavioral decisions
       how the avoidance behavior is mediated by the nervous system

the ear of noctuids consists of a tympanic membrane stretched over an
    enclosed ear sac located on the insect's abdomen
    two sensory (acoustic) neurons contact the tympanic membrane
    the two acoustic neurons are designated A1 and A2, and
       A1 is about 10 times more sensitive to sound that A2
    A1 and A2 are most sensitive to sound in the frequency range from
       40 to 70 kHz, which is in the frequency range of most bat cries

Kenneth Roeder recorded the responses of the acoustic neurons A1 and A2
    in noctuids to the actual cries of free-flying bats
    A1, the more sensitive acoustic neuron, can begin to respond to the
       cry when the bat is 100 - 120ft away
       the A1 response (i.e. it's rate of firing) increases as the bat gets closer
    A2 (the less sensitive) begins to respond as the bat gets even closer
    A1 and A2 fire at the maximum rate when the bat is 15 - 20ft away
    noctuids have two ears, one on either side of the abdomen
       the intensity of the cry is lower on the side of the abdomen opposite
    the bat because the abdomen partially deflects the sound waves
    thus, the response of the ear is stronger on the side from which the bat
       is approaching the moth
    by comparing the relative strengths of the responses of the ears on
       either side, the moth nervous system can determine the
       direction from which the moth is approaching

Kenneth Roeder also studied the avoidance responses of free-flying moths to
    pre-recorded bat cries broadcast over a loud speaker
    they related the type of response to the distance of the moth from the
       loud speaker
    distance greater than 120ft -- the moth makes no response
    distance between 20 and 120ft -- the moth turns and flies directly
       away from the sound
    distance less than 20ft -- the moth executes one of the folloiwng:
       a wild series of seemingly random loops and turns
       fold their wings and dive for the ground
       no response at all
       (rarely) turn and fly directly toward or away from the bat

these moth avoidance maneuvers can be understood in the context of bat
    hunting behavior
    a bat cannot detect a moth beyond about 20ft because at greater
       distances the ultrasonic echo is too weak for the bat to hear
    thus, when a moth hears a bat at a distance of more than 20ft, it's
       likely that the bat has not yet detected it, and the best strategy
       for the moth is simply to turn and fly away from the bat
    however, at a distance of less than 20ft, the bat can detect the moth,
       and at that close range the moth has no chance of out-flying
       the bat because the bat is so much faster
    thus, when a moth hears a bat at a distance of less than 20ft, it's best
       strategy is to execute a series of unpredictable loops, turns,
       dives, and similar maneuvers to try to evade the bat

other types of night-flying insects, such as crickets and lacewings, have also
    developed the ability to detect bat cries and avoid bats
    in one insect (dogbane tiger moth) the response is to emit a sound of
       its own that may, perhaps, confuse the bat by jamming its sonar

neuroethology -- the study of the neural basis of natural behavior
    the term comes from the words neurobiology (the study of the nervous
       system) and ethology (the study of behavior)
    neuroethological studies typically consider the whole animal behaving
       within some environmental context
    typical areas of neuroethological research are communication,
       reproduction, prey capture, and escape
    a neuroethological approach has provided insight into how the moth
       avoidance response is mediated by the moth nervous system
    these neuroethological studies were conducted by Kenneth Roeder,
       who is considered the father of neuroethology

the avoidance response is mediated by interneurons in the moth, that receive
    signals from acoustic neurons A1 and A2, process those signals,
    and organize the appropriate motor response
    these interneurons are called acoustic interneurons and are located in
       the thoracic ganglion
    acoustic interneurons are of two basic types:
       relay neurons -- tonic neurons that respond to a sustained sound
       with a sustained increase in discharge rate, and distribute
       that signal to other neurons in the central nervous system
    pulse marker neurons -- phasic neurons, which respond with
       one or two spikes at the onset of a sound and are then
       silent, code the intensity of the sound by means of
       response latency (louder the sound -- shorter the latency),
       and probably aid in determining sound source direction

although escape responses may seem as stereotyped as reflexes,
   they are in fact flexible and well-suited to circumstances
    this flexibility is the result of neural integration in the CNS
    it is manifested in the directedness of escape movements and in the
       integration of escape behavior with the current behavioral state

Mauthner cell -- giant interneurons that mediated directed escape turns in
   fish (and juvenile amphibians)
    Mauthner cells are arranged in a pair on either side of the brainstem
    each Mauthner cell is excited preferentially by strong vibration
       on the side of the fish on which the Mauthner cell is located
    each Mauthner cell sends a crossed, excitatory projection to the
       motoneurons that control the contractions of the muscles along
       the length of the flank on the opposite side of the fish
    each Mauthner cell on one side inhibits the cell on the opposite side,
       by an electrical process that doesn't involve a chemical synapse
    when a Mauthner cell on one side is excited, it inhibits the Mauthner
       cell on the opposite side, but activates the motoneurons (and so
       the muscles) on the opposite side (flank)
    the result is an intense, rapid turn away from the side on which the
       strong, water-borne vibration is coming
    in addition to exciting the motoneurons on the opposite side, a
       Mauthner cell inhibits the motoneurons on the same side
    thus, a Mauthner cell can over-ride ongoing swimming behavior
    Mauthner activation during swimming resets the swim CPG rhythm

many animals have escape responses that are mediated by giant interneurons
    these include: earthworms, crayfish, and teleost (e.g. trout) fish
    these escape responses are directed in the sense that they rapidly turn
       the animal away from the threatening stimulus
       but these (and other) animals have non-giant escape mechanisms that
       can take over if the giants are removed
    the non-giant escape responses may be a bit slower, but they can
       provide precisely-directed escape for weaker stimuli, and can
       follow escape responses mediated by giants with less intense
       but more controlled behaviors that take the animal to shelter

more complex animals have more complex escape responses
    frogs, for example, will turn and jump away from a large, looming
       stimulus
    but they never jump to exactly the same place twice!
    does this variability result because the frog is uncoordinated?
       maybe not! -- maybe it’s a deliberate attempt to make the exact
       direction of its escape response unpredictable to predators

the escape jump in the locust also shows flexibility
    the locust escape jump has several stages
       first, the tibia is flexed against the femur
       then, the muscles that extend and those that flex the leg are
       contracted simultaneously
    in the flexed position, the flexor muscles have the mechanical
       advantage and keep the locust leg from extending
    to jump, the flexor muscles suddenly relax, leaving the powerful
       extensors free to forcefully extend the leg and hurl the locust
       into the air

two identifiable neurons mediate the escape response in the locust
    the C interneuron helps ensure the co-contraction of the flexor and
       extensor muscles
    the C interneuron is sensitive to weak auditory or tactile stimulation,
       and is activated in response to such stimulation, thus making
       the locust ready for an escape jump
    the M interneuron, which responds to strong auditory or tactile
       stimulation, inhibits the flexor and initiates the jump
    other neurons can also inhibit the flexor and initiate the jump,
       apparently by inhibiting the premotor neurons that excite the
       flexor motoneurons in the first place
    so, two parallel pathways ("M" and "other") can elicit the jump
    escape jumps elicited by the other pathway are more variable

escape responses can be precisely tuned to the current state of the animal
    the escape turn of the cockroach provides an excellent example
    the cockroach detects air disturbances, which may signal large
       approaching objects, by means of its cerci
    cerci -- peg-like appendages at the posterior end of the abdomen that
       are covered with wind sensitive hairs
    sensory afferent neurons transmit signals from cerci hairs to the CNS
    the cerci are essential for the escape response -- covering them with
       Vaseline renders the escape response ineffective
    the cerci sensory afferents contact the giant interneurons
    at first, it was thought that the giant interneurons contacted motoneurons
       directly, forming a fast, disynaptic reflex arc

but three pieces of evidence contradicted this simple view
    cockroach escape could not be mediated by a such a simple reflex
       pathway because:
          first, the delay between cerci stimulation and initiation of escape is
             longer than expected on the basis of such a simple pathway
          second, the giant interneurons don't contact motoneurons directly
          third, the escape response can still be elicited by cerci stimulation
             even after the giant interneurons have been destroyed

careful analysis of cockroach escape showed that this behavior is more
   complex that would be expected for a simple pathway
    for example, the cockroach escape run is preceded by a precise turn
       away from the source of the air disturbance that gives rise to it
    the turn serves to get the cockroach out of the way of danger, like the
       dangerous tongue of a hungry toad
    the wind-sensitive hairs on the cerci are direction selective, and this
       endows the sensory afferents with direction selectivity
    this direction selectivity makes it possible for the cockroach CNS to
       compute precisely the direction from which the wind
       disturbance originates
    the escape turn is also adapted to the current positions and orientations
       of the cockroaches legs

there is a set of about 100 smaller interneurons that make calculations that
   are essential for the escape turn and run in cockroaches
    this large group of interneurons is located in the thoracic ganglion,
       the same ganglion that contains the motoneurons of the leg
       muscles and the giant interneurons
    the smaller interneurons receive input from the cerci sensory afferents
    they determine turn direction and program the turn by adapting it to
       current leg position and orientation
    these smaller interneurons contact leg motoneurons, and also contact
       the giant interneurons
    processing by the smaller interneurons, which transmit the results of
       their processing to the giant interneurons, accounts for the extra
       delay observed in the escape response
    the smaller interneurons mediate the escape response in cockroaches
       in which the giant interneurons have been destroyed
    the set of smaller interneurons also mediates escape to weaker stimuli
       that normally does not involve the giant interneurons